Structure-based interpretation of missense mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass
Abstract
Our understanding of the molecular mechanisms of error-prone lesion bypass has changed dramatically in the past few years. The concept that the key participants in the mutagenic process were accessory proteins that somehow modified the ability of the cell's main replicase to facilitate bypass of normally blocking lesions has been replaced with one in which the replicase is displaced by a polymerase specialized in lesion bypass. The participants in this process remain the same, only their function has been reassigned. What was once known as the UmuC/DinB/Rev1/Rad30 superfamily of mutagenesis proteins, is now known as the Y-family of DNA polymerases. Quite remarkably, within the space of 3 years, the field has advanced from the initial discovery of intrinsic polymerase function, to the determination of the tertiary structures of several Y-family DNA polymerases.A key to determining the biochemical properties of each DNA polymerase is through structure-function studies that result in the site-specific substitution of particular amino acids at critical sites within each DNA polymerase. However, we should not forget the power of genetic selection that allows us to identify residues within each polymerase that are generated by "random mutagenesis" and which are important for both a gain or loss of function in vivo. In this review, we discuss the structural ramifications of several missense mutations previously identified in various Y-family DNA polymerase and speculate on how each amino acid substitution might modify the enzymatic activity of the respective polymerase or possibly perturb protein-protein interactions necessary for efficient translesion replication in vivo.
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These ideas are supported by structural information and by a report that the insertion fidelity of yeast Pol η is severely impaired with difluorotoluene, a nonpolar isosteric analog of thymine that is unable to form Watson-Crick hydrogen bonds with adenine.
“These ideas are supported by structural information (20, 21, 26 -28) and by a report (29) that the insertion fidelity of yeast Pol is severely impaired with difluorotoluene, a nonpolar isosteric analog of thymine that is unable to form Watson-Crick hydrogen bonds with adenine.”
From DNA Replication Fidelity (2004) · cites this paper as [26]
Cites
Nicholls, A. O., Sharp, K. A., & Honig, B. H. (1991) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340110407 · Cited by 5,253 · see citing works
Huang, H., Chopra, R., Verdine, G. L., & Harrison, S. C. (1998) · Science · doi:10.1126/science.282.5394.1669 · Cited by 1,420 · see citing works
The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η
Masutani, C., Kusumoto, R., Yamada, A., Dohmae, N., Yokoi, M., Yuasa, M., Araki, M., Iwai, S., Takio, K., & Hanaoka, F. (1999) · Nature · doi:10.1038/21447 · Cited by 1,292 · see citing works
Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution
Doublié, S., Tabor, S., Long, A. M., Richardson, C. C., & Ellenberger, T. (1998) · Nature · doi:10.1038/34593 · Cited by 1,177 · see citing works
Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA
Krishna, T. S. R., Kong, X., Gary, S. L., Burgers, P., & Kuriyan, J. (1994) · Cell · doi:10.1016/0092-8674(94)90014-0 · Cited by 902 · see citing works
The Y-Family of DNA Polymerases
Ohmori, H., Friedberg, E. C., Fuchs, R. P., Goodman, M. F., Hanaoka, F., Hinkle, D. C., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T., et al. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00278-7 · Cited by 882 · see citing works
DNA Polymerases: Structural Diversity and Common Mechanisms
Steitz, T. A. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.25.17395 · Cited by 848 · see citing works
The complete genome of the crenarchaeon Sulfolobus solfataricus P2
She, Q., Singh, R. K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M., Chan-Weiher, C. C.-Y., Clausen, I. G., Curtis, B. A., Moors, A. D., et al. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141222098 · Cited by 775 · see citing works
Kong, X., Onrust, R., O’Donnell, M. E., & Kuriyan, J. (1992) · Cell · doi:10.1016/0092-8674(92)90445-i · Cited by 754 · see citing works
Efficient Bypass of a Thymine-Thymine Dimer by Yeast DNA Polymerase, Polη
Johnson, R. E., Prakash, S., & Prakash, L. (1999) · Science · doi:10.1126/science.283.5404.1001 · Cited by 736 · see citing works
<i>hRAD30</i> Mutations in the Variant Form of Xeroderma Pigmentosum
Johnson, R. E., Kondratick, C. M., Prakash, S., & Prakash, L. (1999) · Science · doi:10.1126/science.285.5425.263 · Cited by 732 · see citing works
Li, Y., Korolev, S., & Waksman, G. (1998) · The EMBO Journal · doi:10.1093/emboj/17.24.7514 · Cited by 689 · see citing works
Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions
Johnson, R. E., Washington, M. T., Haracska, L., Prakash, S., & Prakash, L. (2000) · Nature · doi:10.1038/35023030 · Cited by 632 · see citing works
Crystal Structure of a Y-Family DNA Polymerase in Action
Ling, H., Boudsocq, F., Woodgate, R., & Yang, W. (2001) · Cell · doi:10.1016/s0092-8674(01)00515-3 · Cited by 610 · see citing works
Self-citationCompilation, alignment, and phylogenetic relationships of DNA polymerases
Braithwaite, D. K., & Ito, J. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.4.787 · Cited by 586 · see citing works
Deoxycytidyl transferase activity of yeast REV1 protein
Nelson, J. R., Lawrence, C. W., & Hinkle, D. C. (1996) · Nature · doi:10.1038/382729a0 · Cited by 573 · see citing works
Kato, T., & Shinoura, Y. (1977) · Molecular and General Genetics MGG · doi:10.1007/bf00283484 · Cited by 569 · see citing works
Structure of the Replicating Complex of a Pol α Family DNA Polymerase
Franklin, M. C., Wang, J., & Steitz, T. A. (2001) · Cell · doi:10.1016/s0092-8674(01)00367-1 · Cited by 538 · see citing works
Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal
Kiefer, J. R., Mao, C., Braman, J. C., & Beese, L. S. (1998) · Nature · doi:10.1038/34693 · Cited by 518 · see citing works
Roles of E. coli DNA polymerases IV and V in lesion-targeted and untargeted SOS mutagenesis
Tang, M., Pham, P., Shen, X., Taylor, J.-S., O'Donnell, M., Woodgate, R., & Goodman, M. F. (2000) · Nature · doi:10.1038/35010020 · Cited by 443 · see citing works
Napolitano, R. L., Janel‐Bintz, R., Wagner, J. E., & Fuchs, R. P. (2000) · The EMBO Journal · doi:10.1093/emboj/19.22.6259 · Cited by 403 · see citing works
Fidelity of Human DNA Polymerase η
Johnson, R. E., Washington, M. T., Prakash, S., & Prakash, L. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.11.7447 · Cited by 399 · see citing works
Low fidelity DNA synthesis by human DNA polymerase-η
Matsuda, T., Bebenek, K., Masutani, C., Hanaoka, F., & Kunkel, T. A. (2000) · Nature · doi:10.1038/35010014 · Cited by 372 · see citing works
Reuven, N. B., Arad, G., Maor-Shoshani, A., & Livneh, Z. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.45.31763 · Cited by 372 · see citing works
Structure of the Catalytic Core of S. cerevisiae DNA Polymerase η
Trincão, J., Johnson, R. E., Escalante, C. R., Prakash, S., Prakash, L., & Aggarwal, A. K. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00306-9 · Cited by 344 · see citing works
Compilation and alignment of DNA polymerase sequences
Ito, J., & Braithwaite, D. K. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.15.4045 · Cited by 337 · see citing works
A universal protein–protein interaction motif in the eubacterial DNA replication and repair systems
Dalrymple, B. P., Kongsuwan, K., Wijffels, G. L., Dixon, N. E., & Jennings, P. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191384398 · Cited by 334 · see citing works
Complete Genome Sequence of an Aerobic Thermoacidophilic Crenarchaeon, Sulfolobus tokodaii strain7
Kawarabayasi, Y. (2001) · DNA Research · doi:10.1093/dnares/8.4.123 · Cited by 327 · see citing works
MUTANTS OF YEAST DEFECTIVE IN MUTATION INDUCED BY ULTRAVIOLET LIGHT
Lemontt, J. F. (1971) · Genetics · doi:10.1093/genetics/68.1.21 · Cited by 325 · see citing works
Crystal Structure of the Processivity Clamp Loader Gamma (γ) Complex of E. coli DNA Polymerase III
Jeruzalmi, D., O’Donnell, M. E., & Kuriyan, J. (2001) · Cell · doi:10.1016/s0092-8674(01)00463-9 · Cited by 322 · see citing works
polι, a remarkably error-prone human DNA polymerase
Tissier, A., McDonald, J. P., Frank, E. G., & Woodgate, R. (2000) · Genes & Development · doi:10.1101/gad.14.13.1642 · Cited by 315 · see citing works
McDonald, J. P., Levine, A. S., & Woodgate, R. (1997) · Genetics · doi:10.1093/genetics/147.4.1557 · Cited by 314 · see citing works
SOS Mutator DNA Polymerase IV Functions in Adaptive Mutation and Not Adaptive Amplification
McKenzie, G. J., Lee, P. L., Lombardo, M.-J., Hastings, P. J., & Rosenberg, S. M. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00204-0 · Cited by 305 · see citing works
Error-free and error-prone lesion bypass by human DNA polymerase kappa in vitro
Zhang, Y. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.21.4138 · Cited by 303 · see citing works
Error-prone bypass of certain DNA lesions by the human DNA polymerase κPreprint
Ohashi, E., Ogi, T., Kusumoto, R., Iwai, S., Masutani, C., Hanaoka, F., & Ohmori, H. (2000) · Genes & Development · doi:10.1101/gad.14.13.1589 · Cited by 279 · see citing works
Kannouche, P., Broughton, B. C., Volker, M., Hanaoka, F., Mullenders, L. H. F., & Lehmann, A. R. (2001) · Genes & Development · doi:10.1101/gad.187501 · Cited by 278 · see citing works
Physical and Functional Interactions of Human DNA Polymerase η with PCNA
Haracska, L., Johnson, R. E., Unk, I., Phillips, B., Hurwitz, J., Prakash, L., & Prakash, S. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.21.7199-7206.2001 · Cited by 235 · see citing works
Uvm mutants of Escherichia coli K 12 deficient in UV mutagenesis
Steinborn, G. (1978) · Molecular and General Genetics MGG · doi:10.1007/bf00270380 · Cited by 234 · see citing works
Boudsocq, F. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.22.4607 · Cited by 232 · see citing works
Self-citationFidelity and Processivity of DNA Synthesis by DNA Polymerase κ, the Product of the Human DINB1 Gene
Ohashi, E., Bębenek, K., Matsuda, T., Feaver, W. J., Gerlach, V. L., Friedberg, E. C., Ohmori, H., & Kunkel, T. A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m005309200 · Cited by 225 · see citing works
UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD'.
Woodgate, R., Rajagopalan, M. R., Lu, C., & Echols, H. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.19.7301 · Cited by 223 · see citing works
Perry, K. L., Elledge, S. J., Mitchell, B. B., Marsh, L., & Walker, G. C. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.13.4331 · Cited by 216 · see citing works
Evidence for a second function forSaccharomyces cerevisiaeRev1p
Nelson, J. R., Gibbs, P., Nowicka, A., Hinkle, D. C., & Lawrence, C. W. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01997.x · Cited by 205 · see citing works
Tang, M., Bruck, I., Eritja, R., Turner, J., Frank, E. G., Woodgate, R., O’Donnell, M. E., & Goodman, M. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.17.9755 · Cited by 202 · see citing works
Preferential Incorporation of G Opposite Template T by the Low-Fidelity Human DNA Polymerase ι
Zhang, Y., Yuan, F., Wu, X., & Wang, Z. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.19.7099-7108.2000 · Cited by 200 · see citing works
Zhou, B.-L., Pata, J. D., & Steitz, T. A. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00310-0 · Cited by 198 · see citing works
Interaction with PCNA Is Essential for Yeast DNA Polymerase η Function
Haracska, L., Kondratick, C. M., Unk, I., Prakash, S., & Prakash, L. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00319-7 · Cited by 198 · see citing works
Targeting of human DNA polymerase ι to the replication machinery via interaction with PCNA
Haracska, L., Johnson, R. E., Unk, I., Phillips, B. B., Hurwitz, J., Prakash, L., & Prakash, S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261560798 · Cited by 193 · see citing works
Archaeal DNA Replication: Identifying the Pieces to Solve a Puzzle
Cann, I., & Ishino, Y. (1999) · Genetics · doi:10.1093/genetics/152.4.1249 · Cited by 193 · see citing works
Gerlach, V. L., Aravind, L., Gotway, G. K., Schultz, R. A., Koonin, E. V., & Friedberg, E. C. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.21.11922 · Cited by 191 · see citing works
Novel Human and Mouse Homologs of Saccharomyces cerevisiae DNA Polymerase η
McDonald, J. P., Rapić-Otrin, V., Epstein, J. A., Broughton, B. C., Wang, X., Lehmann, A. R., Wolgemuth, D. J., & Woodgate, R. (1999) · Genomics · doi:10.1006/geno.1999.5906 · Cited by 183 · see citing works
The human DINB1 gene encodes the DNA polymerase Polθ
Johnson, R. E., Prakash, S., & Prakash, L. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.8.3838 · Cited by 182 · see citing works
Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus.
Silvian, L. F., Toth, E. A., Pham, P., Goodman, M. F., & Ellenberger, T. E. (2001) · Nature Structural Biology · doi:10.1038/nsb1101-984 · Cited by 179 · see citing works
Stimulation of DNA Synthesis Activity of Human DNA Polymerase κ by PCNA
Haracska, L., Unk, I., Johnson, R. E., Phillips, B. B., Hurwitz, J., Prakash, L., & Prakash, S. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.3.784-791.2002 · Cited by 177 · see citing works
Molecular analysis of mutations in DNA polymerase η in xeroderma pigmentosum-variant patients
Broughton, B. C., Cordonnier, A. M., Kleijer, W. J., Jaspers, N. G. J., Fawcett, H., Raams, A., Garritsen, V. H., Stary, A., Avril, M., Boudsocq, F., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.022473899 · Cited by 170 · see citing works
Self-citationThe β clamp targets DNA polymerase IV to DNA and strongly increases its processivity
Wagner, J. E., 藤井, 慎., Grúz, P., Nohmi, T., & Fuchs, R. P. (2000) · EMBO Reports · doi:10.1093/embo-reports/kvd109 · Cited by 168 · see citing works
Regulation of SOS mutagenesis by proteolysis.
Frank, E. G., Ennis, D. G., Gonzalez, M., Levine, A. S., & Woodgate, R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.19.10291 · Cited by 164 · see citing works
Escherichia coli DNA Polymerase IV Mutator Activity: Genetic Requirements and Mutational Specificity
Wagner, J. E., & Nohmi, T. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.16.4587-4595.2000 · Cited by 159 · see citing works
The REV1 gene of Saccharomyces cerevisiae: isolation, sequence, and functional analysis
Larimer, F. W., Perry, J. R., & Hardigree, A. A. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.1.230-237.1989 · Cited by 145 · see citing works
Structural analysis of the umu operon required for inducible mutagenesis in Escherichia coli.
Kitagawa, Y., Akaboshi, E., Shinagawa, H., Horii, T., Ogawa, H., & Kato, T. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.13.4336 · Cited by 137 · see citing works
Roush, A. A., Suarez, M., Friedberg, E. C., Radman, M., & Siede, W. (1998) · Molecular and General Genetics MGG · doi:10.1007/s004380050698 · Cited by 135 · see citing works
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
Sommer, S., Bailone, A., & Devoret, R. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb00968.x · Cited by 126 · see citing works
Unique misinsertion specificity of polι may decrease the mutagenic potential of deaminated cytosines
Vaisman, A., & Woodgate, R. (2001) · The EMBO Journal · doi:10.1093/emboj/20.22.6520 · Cited by 125 · see citing works
Purification and Characterization of polκ, a DNA Polymerase Encoded by the Human DINB1 Gene
Gerlach, V. L., Feaver, W. J., Fischhaber, P. L., & Friedberg, E. C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m004413200 · Cited by 117 · see citing works
Lenne‐Samuel, N., Wagner, J. E., Etienne, H., & Fuchs, R. P. (2002) · EMBO Reports · doi:10.1093/embo-reports/kvf007 · Cited by 116 · see citing works
Specific RecA amino acid changes affect RecA–UmuD′C interaction
Sommer, S., Boudsocq, F., Devoret, R., & Bailone, A. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00803.x · Cited by 113 · see citing works
Self-citationPurification of a Soluble UmuD′C Complex from Escherichia coli
Bruck, I., Woodgate, R., McEntee, K., & Goodman, M. F. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.18.10767 · Cited by 105 · see citing works
Clamp loader structure predicts the architecture of DNA polymerase III holoenzyme and RFC
O’Donnell, M. E., Jeruzalmi, D., & Kuriyan, J. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00559-0 · Cited by 98 · see citing works
Identification of a DinB/UmuC homolog in the archeon Sulfolobus solfataricus
Kulaeva, O. I., Koonin, E. V., McDonald, J. P., Randall, S. K., Rabinovich, N., Connaughton, J. F., Levine, A. S., & Woodgate, R. (1996) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(96)00164-9 · Cited by 91 · see citing works
Ho, C., Kulaeva, O. I., Levine, A. S., & Woodgate, R. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.17.5411-5419.1993 · Cited by 89 · see citing works
The two-step model of bacterial UV mutagenesis
Bridges, B. A., & Woodgate, R. (1985) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(85)90110-1 · Cited by 89 · see citing works
Nohmi, T., Hakura, A., Nakai, Y., Watanabe, M., Murayama, S. Y., & Sofuni, T. (1991) · Journal of Bacteriology · doi:10.1128/jb.173.3.1051-1063.1991 · Cited by 82 · see citing works
Proofreading of DNA Polymerase η-dependent Replication Errors
Bebenek, K., Matsuda, T., Masutani, C., Hanaoka, F., & Kunkel, T. A. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c000690200 · Cited by 76 · see citing works
dinP, a new gene in Escherichia coli, whose product shows similarities to UmuC and its homologues
Ohmori, H., Hatada, E., Qiao, Y., Tsuji, M., & Fukuda, R. (1995) · Mutation Research Letters · doi:10.1016/0165-7992(95)90024-1 · Cited by 74 · see citing works
Characterization of the umu-complementing operon from R391
Kulaeva, O. I., Wootton, J. C., Levine, A. S., & Woodgate, R. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.10.2737-2743.1995 · Cited by 72 · see citing works
Sundin, G. W., Kidambi, S. P., Ullrich, M. S., & Bender, C. L. (1996) · Gene · doi:10.1016/0378-1119(96)00273-9 · Cited by 70 · see citing works
Quantitation of the inhibition of hfr x F− recombination by the mutagenesis complex UmuD′C
Boudsocq, F., Campbell, M., Devoret, R., & Bailone, A. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1098 · Cited by 66 · see citing works
Self-citationSequence analysis and mapping of the Salmonella typhimurium LT2 umuDC operon
Smith, C. M., Koch, W. H., Franklin, S. B., Foster, P. L., Cebula, T. A., & Eisenstadt, E. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.9.4964-4978.1990 · Cited by 62 · see citing works
Yuasa, M., Masutani, C., Eki, T., & Hanaoka, F. (2000) · Oncogene · doi:10.1038/sj.onc.1203842 · Cited by 61 · see citing works
Mutations in human DNA polymerase η motif II alter bypass of DNA lesions
Glick, E., Vigna, K. L., & Loeb, L. A. (2001) · The EMBO Journal · doi:10.1093/emboj/20.24.7303 · Cited by 55 · see citing works
Grúz, P., Pisani, F. M., Shimizu, M., Yamada, M., Hayashi, I., Morikawa, K., & Nohmi, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107213200 · Cited by 55 · see citing works
Modulation of RecA Nucleoprotein Function by the Mutagenic UmuD′C Protein Complex
Rehrauer, W. M., Bruck, I., Woodgate, R., Goodman, M. F., & Kowalczykowski, S. C. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.49.32384 · Cited by 55 · see citing works
Sutton, M. D., & Walker, G. C. (2001) · Journal of Bacteriology · doi:10.1128/jb.183.4.1215-1224.2001 · Cited by 54 · see citing works
Mechanisms of dCMP Transferase Reactions Catalyzed by Mouse Rev1 Protein
Masuda, Y., Takahashi, M., Fukuda, S., Sumii, M., & Kamiya, K. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110149200 · Cited by 53 · see citing works
Human DNA Polymerase ι Promiscuous Mismatch Extension
Vaisman, A., Tissier, A., Frank, E. G., Goodman, M. F., & Woodgate, R. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102694200 · Cited by 51 · see citing works
Structural characterization of the Salmonella typhimurium LT2 umu operon
Thomas, S. M., Crowne, H. M., Pidsley, S. C., & Sedgwick, S. G. (1990) · Journal of Bacteriology · doi:10.1128/jb.172.9.4979-4987.1990 · Cited by 49 · see citing works
In vivo stability of the Umu mutagenesis proteins: a major role for RecA
Frank, E. G., Gonzalez, M., Ennis, D. G., Levine, A. S., & Woodgate, R. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.12.3550-3556.1996 · Cited by 49 · see citing works
Reuven, N. B., Arad, G., Stasiak, A. Z., Stasiak, A., & Livneh, Z. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m006828200 · Cited by 47 · see citing works
Acidic Residues Critical for the Activity and Biological Function of Yeast DNA Polymerase η
Kondratick, C. M., Washington, M. T., Prakash, S., & Prakash, L. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.6.2018-2025.2001 · Cited by 46 · see citing works
Daimon, K., Kawarabayasi, Y., Kikuchi, H., Sako, Y., & Ishino, Y. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.3.687-694.2002 · Cited by 44 · see citing works
Isolation and characterization of novel plasmid-encoded umuC mutants
Woodgate, R., Singh, M., Kulaeva, O. I., Frank, E. G., Levine, A. S., & Koch, W. H. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.16.5011-5021.1994 · Cited by 42 · see citing works
Frank, E. G., Cheng, N., Chat, C., Cerritelli, M. E., Bruck, I., Goodman, M. F., Egelman, E. H., Woodgate, R., & Steven, A. C. (2000) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.3591 · Cited by 41 · see citing works
Escherichia coli umuDC mutants: DNA sequence alterations and UmuD cleavage
Koch, W. H., Ennis, D. G., Levine, A. S., & Woodgate, R. (1992) · Molecular and General Genetics MGG · doi:10.1007/bf00265442 · Cited by 38 · see citing works
Specific amino acid changes enhance the anti‐recombination activity of the UmuD′C complex
Sommer, S., Coste, G., & Bailone, A. (2000) · Molecular Microbiology · doi:10.1046/j.1365-2958.2000.01809.x · Cited by 18 · see citing works
Bates, H. J., Bridges, B. A., & Woodgate, R. (1991) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(91)90176-o · Cited by 16 · see citing works
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Kunkel, T. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.r400006200 · Cited by 754 · see citing works
Formation and Repair of Interstrand Cross-Links in DNA
Noll, D. M., Mason, T. M., & Miller, P. S. (2005) · Chemical Reviews · doi:10.1021/cr040478b · Cited by 485 · 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
Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the β‐clamp
Bunting, K. A., Roe, S. M., & Pearl, L. H. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg568 · Cited by 225 · see citing works
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
Boudsocq, F., Kokoska, R. J., Plosky, B. S., Vaisman, A., Ling, H., Kunkel, T. A., Yang, W., & Woodgate, R. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405249200 · Cited by 138 · see citing works
Self-citationKunkel, T. A., Pavlov, Y. I., & Bebenek, K. (2003) · DNA Repair · doi:10.1016/s1568-7864(02)00224-0 · Cited by 125 · see citing works
Targets for Combating the Evolution of Acquired Antibiotic Resistance
Culyba, M. J., Mo, C. Y., & Kohli, R. M. (2015) · Biochemistry · doi:10.1021/acs.biochem.5b00109 · Cited by 125 · see citing works
Reduction in frataxin causes progressive accumulation of mitochondrial damage
Karthikeyan, G. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg349 · Cited by 102 · see citing works
Antibiotic Resistance Acquired through a DNA Damage-Inducible Response in Acinetobacter baumannii
Norton, M., Spilkia, A. J., & Godoy, V. G. (2013) · Journal of Bacteriology · doi:10.1128/jb.02176-12 · Cited by 96 · see citing works
DNA polymerases and human diseases
Sweasy, J. B., Lauper, J. M., & Eckert, K. A. (2006) · Radiation Research · doi:10.1667/rr0706.1 · Cited by 93 · see citing works
Wong, J. H. Y., Fiala, K. A., Suo, Z., & Ling, H. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.03.038 · Cited by 89 · see citing works
Targeting the DNA damage response for cancer therapy
Powell, S. N., & Bindra, R. S. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.04.011 · Cited by 86 · see citing works
Xeroderma Pigmentosum-Variant Patients from America, Europe, and Asia
Inui, H., Oh, K., Nadem, C., Ueda, T., Khan, S. G., Metın, A., Gözükara, E. M., Emmert, S., Slor, H., Busch, D. B., et al. (2008) · Journal of Investigative Dermatology · doi:10.1038/jid.2008.48 · Cited by 87 · see citing works
Palm Mutants in DNA Polymerases α and η Alter DNA Replication Fidelity and Translesion Activity
Niimi, A., Limsirichaikul, S., Yoshida, S., Iwai, S., Masutani, C., Hanaoka, F., Kool, E. T., Nishiyama, Y., & Suzuki, M. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.7.2734-2746.2004 · Cited by 84 · see citing works
Godoy, V. G., Jarosz, D. F., Walker, F. L., Simmons, L. A., & Walker, G. C. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7600986 · Cited by 82 · see citing works
The Biochemical Requirements of DNA Polymerase V-mediated Translesion Synthesis Revisited
藤井, 慎., Gasser, V., & Fuchs, R. P. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.06.017 · Cited by 75 · see citing works
The dinB Operon and Spontaneous Mutation in Escherichia coli
McKenzie, G. J., Magner, D. B., Lee, P. L., & Rosenberg, S. M. (2003) · Journal of Bacteriology · doi:10.1128/jb.185.13.3972-3977.2003 · Cited by 72 · see citing works
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 · see citing works
Properties and Functions of Escherichia Coli: Pol IV and Pol V
Fuchs, R. P., Fujii, S., & Wagner, J. (2004) · Advances in Protein Chemistry · doi:10.1016/s0065-3233(04)69008-5 · Cited by 100 · see citing works
Kusumoto, R., Masutani, C., Shimmyo, S., Iwai, S., & Hanaoka, F. (2004) · Genes to Cells · doi:10.1111/j.1365-2443.2004.00797.x · Cited by 69 · see citing works
Functions of Eukaryotic DNA Polymerases
Shcherbakova, P. V., Bębenek, K., & Kunkel, T. A. (2003) · Science of Aging Knowledge Environment · doi:10.1126/sageke.2003.8.re3 · Cited by 69 · see citing works
Vaisman, A., Frank, E. G., Iwai, S., Ohashi, E., Ohmori, H., Hanaoka, F., & Woodgate, R. (2003) · DNA repair · doi:10.1016/s1568-7864(03)00094-6 · Cited by 59 · see citing works
Yuasa, M., Masutani, C., Hirano, A., Cohn, M. A., Yamaizumi, M., Nakatani, Y., & Hanaoka, F. (2006) · Genes to Cells · doi:10.1111/j.1365-2443.2006.00974.x · Cited by 57 · see citing works
Considering the cancer consequences of altered DNA polymerase function
Kunkel, T. A. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00027-8 · Cited by 55 · see citing works
Seo, K. Y., Nagalingam, A., Miri, S., Yin, J., Chandani, S., Kolbanovskiy, A., Shastry, A., & Loechler, E. L. (2006) · DNA repair · doi:10.1016/j.dnarep.2005.12.009 · Cited by 51 · see citing works
Niwa, O. (2003) · Oncogene · doi:10.1038/sj.onc.1207037 · Cited by 50 · see citing works
Two processivity clamp interactions differentially alter the dual activities of UmuC
Beuning, P. J., Sawicka, D., Barsky, D., & Walker, G. C. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04959.x · Cited by 45 · see citing works
Vaisman, A., Kuban, W., McDonald, J. P., Karata, K., Yang, W., Goodman, M. F., & Woodgate, R. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks233 · Cited by 43 · see citing works
Whole-Exome Sequencing Enables Rapid Determination of Xeroderma Pigmentosum Molecular Etiology
Ortega‐Recalde, O., Vergara, J. I., Fonseca, D. J., Ríos, X. P., Mosquera, H., Bermúdez, O. M., Medina, C. L., Vargas, C. I., Pallares, A. E., Restrepo, C. M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0064692 · Cited by 39 · see citing works
A RecA Protein Surface Required for Activation of DNA Polymerase V
Gruber, A. J., Erdem, A. L., Sabat, G., Karata, K., Jaszczur, M. M., Vo, D. D., Olsen, T. M., Woodgate, R., Goodman, M. F., & Cox, M. M. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005066 · Cited by 37 · see citing works
Sherrer, S. M., Fiala, K. A., Fowler, J. D., Newmister, S. A., Pryor, J. M., & Suo, Z. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq719 · Cited by 36 · see citing works
Perlow-Poehnelt, R. A., Likhterov, I., Scicchitano, D. A., Geacintov, N. E., & Broyde, S. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404332200 · Cited by 35 · see citing works
Escherichia coli Y family DNA polymerases
Jason, M. (2011) · Frontiers in bioscience · doi:10.2741/3904 · Cited by 32 · see citing works
Lee, C. H., Chandani, S., & Loechler, E. L. (2006) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2005.10.009 · Cited by 30 · see citing works
Zhang, H., Rhee, C., Bębenek, A., Drake, J. W., Wang, J., & Konigsberg, W. H. (2006) · Biochemistry · doi:10.1021/bi052099y · Cited by 27 · see citing works
Kinetic Analysis of the Bypass of a Bulky DNA Lesion Catalyzed by Human Y-Family DNA Polymerases
Sherrer, S. M., Sanman, L. E., Xia, C. X., Bolin, E. R., Malik, C. K., Efthimiopoulos, G., Basu, A. K., & Suo, Z. (2012) · Chemical Research in Toxicology · doi:10.1021/tx200531y · Cited by 27 · see citing works
Pednekar, V., Weerasooriya, S., Jasti, V. P., & Basu, A. K. (2014) · Chemical Research in Toxicology · doi:10.1021/tx4002786 · Cited by 25 · see citing works
Yin, J., Seo, K. Y., & Loechler, E. L. (2004) · DNA repair · doi:10.1016/j.dnarep.2003.11.012 · Cited by 25 · see citing works
Seo, K., Nagalingam, A., Tiffany, M. R., & Loechler, E. L. (2005) · Mutagenesis · doi:10.1093/mutage/gei061 · Cited by 25 · see citing works
Zhang, H., Beckman, J. W., Wang, J., & Konigsberg, W. H. (2009) · Biochemistry · doi:10.1021/bi900422b · Cited by 24 · see citing works
Biochemical analysis of active site mutations of human polymerase η
Suarez, S. C., Beardslee, R. A., Toffton, S. M., & McCulloch, S. D. (2013) · Mutation research · doi:10.1016/j.mrfmmm.2013.03.001 · Cited by 22 · see citing works
Multiple solutions to inefficient lesion bypass by T7 DNA polymerase
McCulloch, S. D., & Kunkel, T. A. (2006) · DNA repair · doi:10.1016/j.dnarep.2006.06.003 · Cited by 21 · see citing works
Bartl, S., Miracle, A. L., Rumfelt, L. L., Kepler, T. B., Mochon, E., Litman, G. W., & Flajnik, M. F. (2003) · Immunogenetics · doi:10.1007/s00251-003-0608-3 · Cited by 21 · see citing works
Hawver, L. A., Gillooly, C. A., & Beuning, P. J. (2011) · Journal of Bacteriology · doi:10.1128/jb.05301-11 · Cited by 18 · see citing works
Steric Gate Variants of UmuC Confer UV Hypersensitivity on Escherichia coli
Shurtleff, B. W., Ollivierre, J. N., Tehrani, M., Walker, G. C., & Beuning, P. J. (2009) · Journal of Bacteriology · doi:10.1128/jb.01742-08 · Cited by 19 · see citing works
Contribution of increased mutagenesis to the evolution of pollutants-degrading indigenous bacteria
Ilmjärv, T., Naanuri, E., & Kivisaar, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182484 · Cited by 20 · see citing works
Better living with hyper‐mutation
Goodman, M. F. (2016) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22023 · Cited by 17 · see citing works
Chandani, S., & Loechler, E. L. (2006) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2006.05.003 · Cited by 17 · see citing works
Genomic analysis of cancer tissue reveals that somatic mutations commonly occur in a specific motif
Makridakis, N. M., Ferraz, L. F. C., & Reichardt, J. K. V. (2008) · Human Mutation · doi:10.1002/humu.20810 · Cited by 16 · see citing works
Glick, E., Chau, J. S., Vigna, K. L., McCulloch, S. D., Adman, E. T., Kunkel, T. A., & Loeb, L. A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300686200 · Cited by 16 · see citing works
Seo, K. Y., Yin, J., Donthamsetti, P., Chandani, S., Lee, C. H., & Loechler, E. L. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.07.016 · Cited by 14 · see citing works
Beuning, P. J., Chan, S., Waters, L. S., Addepalli, H., Ollivierre, J. N., & Walker, G. C. (2009) · Journal of Bacteriology · doi:10.1128/jb.00292-09 · Cited by 14 · see citing works
Sherrer, S. M., Taggart, D. J., Pack, L. R., Malik, C. K., Basu, A. K., & Suo, Z. (2012) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2012.08.002 · Cited by 13 · see citing works
Increased Flexibility Enhances Misincorporation
Perlow-Poehnelt, R. A., Likhterov, I., Wang, L., Scicchitano, D. A., Geacintov, N. E., & Broyde, S. B. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606769200 · Cited by 13 · see citing works
Comparative Molecular Dynamics Studies of Human DNA Polymerase η
Ucisik, M. N., & Hammes‐Schiffer, S. (2015) · Journal of Chemical Information and Modeling · doi:10.1021/acs.jcim.5b00606 · Cited by 12 · see citing works
Beardslee, R. A., Suarez, S. C., Toffton, S. M., & McCulloch, S. D. (2013) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21807 · Cited by 9 · see citing works
Hawver, L. A., Tehrani, M., Antczak, N. M., Kania, D., Muser, S., Sefcikova, J., & Beuning, P. J. (2015) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2015.07.003 · Cited by 7 · see citing works
Sommer, S., Bécherel, O. J., Coste, G., Bailone, A., & Fuchs, R. P. (2003) · DNA repair · doi:10.1016/j.dnarep.2003.08.008 · Cited by 7 · see citing works
Xie, P. (2011) · Theoretical Biology and Medical Modelling · doi:10.1186/1742-4682-8-22 · Cited by 6 · see citing works
Wang, L., Liang, C., Wu, J., Liu, L., & Tyo, K. E. J. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.01013-17 · Cited by 6 · see citing works
Polymerase Switching in Response to DNA Damage
Ollivierre, J. N., Silva, M. C., Sefcikova, J., & Beuning, P. J. (2010) · Biological and medical physics series · doi:10.1007/978-0-387-92808-1_11 · Cited by 5 · see citing works
Lee, C. H., & Loechler, E. L. (2003) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(03)00107-6 · Cited by 5 · see citing works
Effect of pH on the Misincorporation Rate of DNA Polymerase η
Nishimoto, N., Suzuki, M., & Izuta, S. (2016) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b15-00900 · Cited by 4 · see citing works
Krwawicz, J., Czajkowska, A., Felczak, M. M., & Pietrzykowska, I. (2003) · Acta Biochimica Polonica · doi:10.18388/abp.2003_3624 · Cited by 1 · see citing works
Interstrand Crosslinks - Induction and repair
Vare, D. (2012) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Acinetobacter baumannii DNA Damage-Inducible Response in Antibiotic Resistance Acquired through a
Norton, M., Spilkia, A. J., & Godoy, V. G. (2013)
Investigating the role of UmuD in DNA polymerase regulation
Silva, M. C. (2009) · doi:10.17760/d20000055
Assessment And In Vitro Repair Of Damaged Dna Templates From Forensic Stains
Hall, A. (2005) · Journal of International Crisis and Risk Communication Research
DNA repair | UmuDC Lesion Bypass DNA Polymerase V
Beuning, P. J., Stern, H. R., & Dilworth, R. J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.21484-2
Faculty Opinions recommendation of The dinB operon and spontaneous mutation in Escherichia coli.
Friedberg, E. C. (2003) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1014044.192545
DNA repair | XPV Polymerase and the Bypass of Ultraviolet DNA Damage
Sabbioneda, S. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819460-7.00130-4
Conserved Active Site Loop Residues of E. coli DinB and Human DNA Polymerase Kappa Govern Activity
Antczak, N. M., Ippoliti, P. J., Ahn, J., Kankanamge, L. S. P., Dudko, T., Balfour‐Jeffrey, K., Pancoe, B., MacDiarmid, Z., Pham, C. M., David, W., et al. (2026) · Environmental and Molecular Mutagenesis · doi:10.1002/em.70075
DNA damage and repair: Future perspectives
Rajpurohit, Y. S., Mishra, A., Sharma, D. K., & Soni, I. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-42857-9.00002-5
Protein-Nucleic Acid Interactions in Nuclease and Polymerases
Abdur, R. (2022) · UPT. Syiah Kuala University Library (Syiah Kuala University) · doi:10.57709/2005101
- Authors
- Boudsocq, F.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Boudsocq, F
- Venue
- DNA Repair
- Publisher
- Elsevier BV
- Published
- 2002-05-30
- Volume
- 1
- Issue
- 5
- Pages
- 343-358
- ISSN
- 1568-7856 (ISSN-L)
- 1568-7864
- OpenAlex
- W2056808794
- Cited by
- 79
- References
- 96
- Citations by year
- 2026: 2 · 2022: 1 · 2021: 1 · 2020: 1 · 2017: 2 · 2016: 2 · 2015: 4 · 2014: 1 · 2013: 8 · 2012: 6
- FWCI
- 3.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- DNA repair (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute for Health and Care Research
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Physical Sciences › Materials Science › Materials Chemistry › Enzyme Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Keywords
- Y-family DNA polymerases, missense mutations, translesion synthesis, error-prone DNA replication, lesion bypass, structure-function relationship, protein tertiary structure, amino acid substitutions, protein-protein interaction
- MeSH terms
- Amino Acid Sequence, Animals, DNA Damage, DNA-Directed DNA Polymerase, DNA Repair, DNA Replication, Escherichia coli, Multigene Family, Humans, Models, Genetic, Molecular Sequence Data, Protein Conformation, Structure-Activity Relationship, Sequence Homology, Amino Acid, Protein Folding, Amino Acid Substitution, Mutation, Missense
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