Participation of DNA polymerase ζ in replication of undamaged DNA in Saccharomyces cerevisiae

Genetics

Volumn 184, Issue 1, 2010, Pages 27-42

  Northam, Matthew R ^a   Robinson, Heather A ^a,b   Kochenova, Olga V ^a,c   Shcherbakova, Polina V ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Sam Houston State University   (United States)

^c ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE ZETA; REPLISOME; UNCLASSIFIED DRUG;

ANAEROBIC GROWTH; ARTICLE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ESCHERICHIA COLI; FUNGAL STRAIN; GENE REPLICATION; IN VITRO STUDY; MUTAGENESIS; MUTATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; WILD TYPE; YEAST CELL;

BASE SEQUENCE; DNA DAMAGE; DNA REPLICATION; DNA, FUNGAL; DNA-DIRECTED DNA POLYMERASE; HYDROXYUREA; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; MUTAGENESIS; MUTATION; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 74249092035     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.107482     Document Type: Article

References (102)

1. ACHARYA, N., R. E. JOHNSON, S. PRAKASH and L. PRAKASH, 2006 Complex formation with Rev1 enhances the proficiency of Saccharomyces cerevisiae DNA polymerase ζ for mismatch extension and for extension opposite from DNA lesions. Mol. Cell. Biol. 26: 9555-9563.
2. ACHARYA, N., R. E. JOHNSON, V. PAGES, L. PRAKASH and S. PRAKASH, 2009 Yeast Rev1 protein promotes complex formation of DNA polymerase ζ with Pol32 subunit of DNA polymerase δ. Proc. Natl. Acad. Sci. USA 106: 9631-9636.
3. AUERBACH, P., R. A. BENNETT, E. A. BAILEY, H. E. KROKAN and B. DEMPLE, 2005 Mutagenic specificity of endogenously generated abasic sites in Saccharomyces cerevisiae chromosomal DNA. Proc. Natl. Acad. Sci. USA 102: 17711-17716.
4. BENNETT, R. A., 1999 The Saccharomyces cerevisiae ETH1 gene, an inducible homolog of exonuclease III that provides resistance to DNA-damaging agents and limits spontaneous mutagenesis. Mol. Cell. Biol. 19: 1800-1809.
5. BERTRAND, P., D. X. TISHKOFF, N. FILOSI, R. DASGUPTA and R. D. KOLODNER, 1998 Physical interaction between components of DNA mismatch repair and nucleotide excision repair. Proc. Natl. Acad. Sci. USA 95: 14278-14283.
6. BOEKE, J. D., F. LACROUTE and G. R. FINK, 1984 A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197: 345-346.
7. BRESSON, A., and R. P. FUCHS, 2002 Lesion bypass in yeast cells: Pol η participates in a multi-DNA polymerase process. EMBO J. 21: 3881-3887.
8. BROOMFIELD, S., B. L. CHOW and W. XIAO, 1998 MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway. Proc. Natl. Acad. Sci. USA 95: 5678-5683.
9. CASSIER, C., R. CHANET, J. A. HENRIQUES and E. MOUSTACCHI, 1980 The effects of three PSO genes on induced mutagenesis: a novel class of mutationally defective yeast. Genetics 96: 841-857.
10. DATTA, A., and S. JINKS-ROBERTSON, 1995 Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268: 1616-1619.
11. DAVIES, A. A., D. HUTTNER, Y. DAIGAKU, S. CHEN and H. D. ULRICH, 2008 Activation of ubiquitin-dependent DNA damage bypass is mediated by replication protein A. Mol. Cell 29: 625-636.
12. D'ERRICO, M., E. PARLANTI and E. DOGLIOTTI, 2008 Mechanism of oxidative DNA damage repair and relevance to human pathology. Mutat. Res. 659: 4-14.
13. DIXON, W. J., and F. J. MASSEY, JR., 1969 Introduction to Statistical Analysis. McGraw-Hill, New York.
14. DRAKE, J.W., 1991 A constant rate of spontaneous mutation in DNA-based microbes. Proc. Natl. Acad. Sci. USA 88: 7160-7164.
15. FIJALKOWSKA, I. J., R. L. DUNN and R. M. SCHAAPER, 1997 Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J. Bacteriol. 179: 7435-7445.
16. FORTUNE, J. M., Y. I. PAVLOV, C. M. WELCH, E. JOHANSSON, P. M. BURGERS et al., 2005 Saccharomyces cerevisiae DNA polymerase δ: high fidelity for base substitutions but lower fidelity for single- and multi-base deletions. J. Biol. Chem. 280: 29980-29987.
17. GARG, P., and P. M. BURGERS, 2005 Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases η and REV1. Proc. Natl. Acad. Sci. USA 102: 18361-18366.
18. GARG, P., C. M. STITH, J. MAJKA and P. M. BURGERS, 2005 Proliferating cell nuclear antigen promotes translesion synthesis by DNA polymerase ζ. J. Biol. Chem. 280: 23446-23450.
19. GELLON, L., R. BARBEY, P. AUFFRET VAN DER KEMP, D. THOMAS and S. BOITEUX, 2001 Synergism between base excision repair, mediated by the DNA glycosylases Ntg1 and Ntg2, and nucleotide excision repair in the removal of oxidatively damaged DNA bases in Saccharomyces cerevisiae. Mol. Genet. Genomics 265: 1087-1096.
20. GIBBS, P. E., and C. W. LAWRENCE, 1995 Novel mutagenic properties of abasic sites in Saccharomyces cerevisiae. J. Mol. Biol. 251: 229-236.
21. GIBBS, P. E., A. BORDEN and C. W. LAWRENCE, 1995 The T-T pyrimidine (6-4) pyrimidinone UV photoproduct is much less mutagenic in yeast than in Escherichia coli. Nucleic Acids Res. 23: 1919-1922.
22. GIBBS, P. E., J. MCDONALD, R. WOODGATE and C. W. LAWRENCE, 2005 The relative roles in vivo of Saccharomyces cerevisiae Pol η, Pol ζ, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer. Genetics 169: 575-582.
23. GLASSNER, B. J., L. J. RASMUSSEN, M. T. NAJARIAN, L.M. POSNICK and L. D. SAMSON, 1998 Generation of a strong mutator phenotype in yeast by imbalanced base excision repair. Proc. Natl. Acad. Sci. USA 95: 9997-10002.
24. GORDENIN, D. A., Y. Y. PROSCYAVICHUS, A. L. MALKOVA, M. V. TROFIMOVA and A. PETERZEN, 1991 Yeast mutants with increased bacterial transposon Tn5 excision. Yeast 7: 37-50.
25. GORDENIN, D. A., K. S. LOBACHEV, N. P. DEGTYAREVA, A. L. MALKOVA, E. PERKINS et al., 1993 Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol. 13: 5315-5322.
26. GUO, C., T. S. TANG, M. BIENKO, J. L. PARKER, A. B. BIELEN et al., 2006 Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol. Cell. Biol. 26: 8892-8900.
27. GUO, D., X. WU, D. K. RAJPAL, J. S. TAYLOR and Z. WANG, 2001 Translesion synthesis by yeast DNA polymerase ζ from templates containing lesions of ultraviolet radiation and acetylaminofluorene. Nucleic Acids Res. 29: 2875-2883.
28. GUO, Y., L. L. BREEDEN, H. ZARBL, B. D. PRESTON and D. L. EATON, 2005 Expression of a human cytochrome p450 in yeast permits analysis of pathways for response to and repair of aflatoxin-induced DNA damage. Mol. Cell. Biol. 25: 5823-5833.
29. GUZDER, S. N., P. SUNG, L. PRAKASH and S. PRAKASH, 1993 Yeast DNA-repair gene RAD14 encodes a zinc metalloprotein with affinity for ultraviolet-damaged DNA. Proc. Natl. Acad. Sci. USA 90: 5433-5437.
30. HARACSKA, L., I. UNK, R. E. JOHNSON, E. JOHANSSON, P. M. BURGERS et al., 2001 Roles of yeast DNA polymerases δ and ζ and of Rev1 in the bypass of abasic sites. Genes Dev. 15: 945-954.
31. HARFE, B. D., and S. JINKS-ROBERTSON, 2000 DNA polymerase ζ introduces multiple mutations when bypassing spontaneous DNA damage in Saccharomyces cerevisiae. Mol. Cell 6: 1491-1499.
32. HOEGE, C., B. PFANDER, G. L. MOLDOVAN, G. PYROWOLAKIS and S. JENTSCH, 2002 RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419: 135-141.
33. HOLBECK, S. L., and J. N. STRATHERN, 1997 A role for REV3 in mutagenesis during double-strand break repair in Saccharomyces cerevisiae. Genetics 147: 1017-1024.
34. HUANG, M. E., A. G. RIO, M. D. GALIBERT and F. GALIBERT, 2002 Pol32, a subunit of Saccharomyces cerevisiae DNA polymerase δ, suppresses genomic deletions and is involved in the mutagenic bypass pathway. Genetics 160: 1409-1422.
35. JOHNSON, R. E., C. A. TORRES-RAMOS, T. IZUMI, S.MITRA, S. PRAKASH et al., 1998 Identification of APN2, the Saccharomyces cerevisiae homolog of the major human AP endonuclease HAP1, and its role in the repair of abasic sites. Genes Dev. 12: 3137-3143.
36. JOHNSON, R. E., M. T. WASHINGTON, L.HARACSKA, S. PRAKASH and L. PRAKASH, 2000 Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature 406: 1015-1019.
37. KAI, M., and T. S. WANG, 2003 Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 17: 64-76.
38. KANG, X. L., F. YADAO, R. D. GIETZ and B. A. KUNZ, 1992 Elimination of the yeast RAD6 ubiquitin conjugase enhances base-pair transitions and G.C → T.A transversions as well as transposition of the Ty element: implications for the control of spontaneous mutation. Genetics 130: 285-294.
39. KANNOUCHE, P. L., J. WING and A. R. LEHMANN, 2004 Interaction of human DNA polymerase η with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14: 491-500.
40. KING, N. M., N. NIKOLAISHVILI-FEINBERG, M. F. BRYANT, D. D. LUCHE, T. P. HEFFERNAN et al., 2005 Overproduction of DNA polymerase η does not raise the spontaneous mutation rate in diploid human fibroblasts. DNA Repair 4: 714-724.
41. KOREN, A., 2007 The role of the DNA damage checkpoint in regulation of translesion DNA synthesis. Mutagenesis 22: 155-160.
42. KOZMIN, S. G., Y. I. PAVLOV, T. A. KUNKEL and E. SAGE, 2003 Roles of Saccharomyces cerevisiae DNA polymerases Polη and Polζ in response to irradiation by simulated sunlight. Nucleic Acids Res. 31: 4541-4552.
43. KOZMIN, S., G. SLEZAK, A. REYNAUD- ANGELIN, C. ELIE, Y. DE RYCKE et al., 2005 UVA radiation is highly mutagenic in cells that are unable to repair 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 102: 13538-13543.
44. LAWRENCE, C. W., and V. M. MAHER, 2001 Mutagenesis in eukaryotes dependent on DNA polymerase ζ and Rev1p. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 41-46.
45. LEE, G. S., E. A. SAVAGE, R. G. RITZEL and R. C. VON BORSTEL, 1988 The base-alteration spectrum of spontaneous and ultraviolet radiation-induced forward mutations in the URA3 locus of Saccharomyces cerevisiae. Mol. Gen. Genet. 214: 396-404.
46. LI, L., K. M. MURPHY, U. KANEVETS and L. J. REHA-KRANTZ, 2005 Sensitivity to phosphonoacetic acid: a new phenotype to probe DNA polymerase δ in Saccharomyces cerevisiae. Genetics 170: 569-580.
47. LOPES, M., M. FOIANI and J. M. SOGO, 2006 Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21: 15-27.
48. MATSUDA, T., K. BEBENEK, C.MASUTANI, F. HANAOKA and T. A. KUNKEL, 2000 Low fidelity DNA synthesis by human DNA polymerase-η. Nature 404: 1011-1013.
49. MITO, E., J. V.MOKHNATKIN,M. C. STEELE, V. L. BUETTNER, S. S. SOMMER et al., 2008 Mutagenic and recombinagenic responses to defective DNA polymerase δ are facilitated by the Rev1 protein in pol3-t mutants of Saccharomyces cerevisiae. Genetics 179: 1795-1806.
50. MORRISON, A., H. ARAKI, A. B. CLARK, R. K. HAMATAKE and A. SUGINO, 1990 A third essential DNA polymerase in S. cerevisiae. Cell 62: 1143-1151.
51. MORRISON, A., J. B. BELL, T. A. KUNKEL and A. SUGINO, 1991 Eukaryotic DNA polymerase amino acid sequence required for 3′→5′ exonuclease activity. Proc. Natl. Acad. Sci. USA 88: 9473-9477.
52. NAIR, D. T., R. E. JOHNSON, L. PRAKASH, S. PRAKASH and A. K. AGGARWAL, 2005 Rev1 employs a novel mechanism of DNA synthesis using a protein template. Science 309: 2219-2222.
53. NELSON, J. R., C. W. LAWRENCE and D. C. HINKLE, 1996 Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272: 1646-1649.
54. NI, T. T., G. T. MARSISCHKY and R. D. KOLODNER, 1999 MSH2 and MSH6 are required for removal of adenine misincorporated opposite 8-oxo-guanine in S. cerevisiae. Mol. Cell 4: 439-444.
55. NICK MCELHINNY, S. A., C. M. STITH, P. M. BURGERS and T. A. KUNKEL, 2007 Inefficient proofreading and biased error rates during inaccurate DNA synthesis by a mutant derivative of Saccharomyces cerevisiae DNA polymerase δ. J. Biol. Chem. 282: 2324-2332.
56. NIIMI, A., S. LIMSIRICHAIKUL, S. YOSHIDA, S. IWAI, C. MASUTANI et al., 2004 Palm mutants in DNA polymerases α and η alter DNA replication fidelity and translesion activity. Mol. Cell. Biol. 24: 2734-2746.
57. NORTHAM, M. R., P. GARG, D. M. BAITIN, P. M. BURGERS and P. V. SHCHERBAKOVA, 2006 A novel function of DNA polymerase ζ regulated by PCNA. EMBO J. 25: 4316-4325.
58. PAVLOV, Y. I., D. NGUYEN and T. A. KUNKEL, 2001a Mutator effects of overproducing DNA polymerase η (Rad30) and its catalytically inactive variant in yeast. Mutat. Res. 478: 129-139.
59. PAVLOV, Y. I., P. V. SHCHERBAKOVA and T. A. KUNKEL, 2001b In vivo consequences of putative active site mutations in yeast DNA polymerases α, ε, δ and ζ. Genetics 159: 47-64.
60. PAVLOV, Y. I., C. S. NEWLON and T. A. KUNKEL, 2002 Yeast origins establish a strand bias for replicational mutagenesis. Mol. Cell 10: 207-213.
61. PAVLOV, Y. I., P. V. SHCHERBAKOVA and I. B. ROGOZIN, 2006 Roles of DNA polymerases in replication, repair, and recombination in eukaryotes. Int. Rev. Cytol. 255: 41-132.
62. POPOFF, S. C., A. I. SPIRA, A.W. JOHNSON and B. DEMPLE, 1990 Yeast structural gene (APN1) for the major apurinic endonuclease: homology to Escherichia coli endonuclease IV. Proc. Natl. Acad. Sci. USA 87: 4193-4197.
63. PRAKASH, S., and L. PRAKASH, 2002 Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev. 16: 1872-1883.
64. PRAKASH, S., R. E. JOHNSON and L. PRAKASH, 2005 Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74: 317-353.
65. PURSELL, Z. F., I. ISOZ, E. B. LUNDSTROM, E. JOHANSSON and T. A. KUNKEL, 2007 Yeast DNA polymerase e participates in leading-strand DNA replication. Science 317: 127-130.
66. QUAH, S. K., R. C. VON BORSTEL and P. J. HASTINGS, 1980 The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics 96: 819-839.
67. RATTRAY, A. J., B. K. SHAFER, C. B. MCGILL and J. N. STRATHERN, 2002 The roles of REV3 and RAD57 in double-strand-break-repair-induced mutagenesis of Saccharomyces cerevisiae. Genetics 162: 1063-1077.
68. ROCHE, H., R. D. GIETZ and B. A. KUNZ, 1994 Specificity of the yeast rev3Δ antimutator and REV3 dependency of the mutator resulting from a defect (rad1Δ) in nucleotide excision repair. Genetics 137: 637-646.
69. ROCHE, H., R. D. GIETZ and B. A. KUNZ, 1995 Specificities of the Saccharomyces cerevisiae rad6, rad18 and rad52 mutators exhibit different degrees of dependence on the REV3 gene product, a putative nonessential DNA polymerase. Genetics 140: 443-456.
70. ROSE, M.D., F.WINSTON and P. HIETER, 1990 Methods in Yeast Genetics.
71. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
72. SCHELLER, J., A. SCHURER, C. RUDOLPH, S.HETTWER and W. KRAMER, 2000 MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155: 1069-1081.
73. SHCHERBAKOVA, P. V., and I. J. FIJALKOWSKA, 2006 Translesion synthesis DNA polymerases and control of genome stability. Front. Biosci. 11: 2496-2517.
74. SHCHERBAKOVA, P. V., and T. A. KUNKEL, 1999 Mutator phenotypes conferred by MLH1 overexpression and by heterozygosity for mlh1 mutations. Mol. Cell. Biol. 19: 3177-3183.
75. SHCHERBAKOVA, P. V., V. N. NOSKOV, M. R. PSHENICHNOV and Y. I. PAVLOV, 1996 Base analog 6-N-hydroxylaminopurine mutagenesis in the yeast S. cerevisiae is controlled by replicative DNA polymerases. Mutat. Res. 369: 33-44.
76. SHCHERBAKOVA, P. V., Y. I. PAVLOV, O. CHILKOVA, I. B. ROGOZIN, E. JOHANSSON et al., 2003 Unique error signature of the four-subunit yeast DNA polymerase ε. J. Biol. Chem. 278: 43770-43780.
77. SIMHADRI, S., P. KRAMATA, B. ZAJC, J. M. SAYER, D. M. JERINA et al., 2002 Benzo[a]pyrene diol epoxide-deoxyguanosine adducts are accurately bypassed by yeast DNA polymerase ζ in vitro. Mutat. Res. 508: 137-145.
78. SIMON, M., L. GIOT and G. FAYE, 1991 The 3′ to 5′ exonuclease activity located in the DNA polymerase d subunit of Saccharomyces cerevisiae is required for accurate replication. EMBO J. 10: 2165-2170.
79. SOGO, J. M., M. LOPES and M. FOIANI, 2002 Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 296: 599-602.
80. SUZUKI, M., A. NIIMI, S. LIMSIRICHAIKUL, S. TOMIDA, Q. M. HUANG et al., 2009 PCNA mono-ubiquitination and activation of translesion DNA polymerases by DNA polymerase α. J. Biochem. 146: 13-21.
81. SWAN, M. K., R. E. JOHNSON, L. PRAKASH, S. PRAKASH and A. K. AGGARWAL, 2009a Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase δ. Nat. Struct. Mol. Biol. 16: 979-986.
82. SWAN, M. K., R. E. JOHNSON, L. PRAKASH, S. PRAKASH and A. K. AGGARWAL, 2009b Structure of the human Rev1-DNA-dNTP ternary complex. J. Mol. Biol. 390: 699-709.
83. SWANSON, R. L., N. J. MOREY, P. W. DOETSCH and S. JINKS-ROBERTSON, 1999 Overlapping specificities of base excision repair, nucleotide excision repair, recombination, and translesion synthesis pathways for DNA base damage in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 2929-2935.
84. TISHKOFF, D. X., N. FILOSI, G. M. GAIDA and R. D. KOLODNER, 1997 A novel mutation avoidance mechanism dependent on S. cerevisiae RAD27 is distinct from DNA mismatch repair. Cell 88: 253-263.
85. TORRES-RAMOS, C. A., R. E. JOHNSON, L. PRAKASH and S. PRAKASH, 2000 Evidence for the involvement of nucleotide excision repair in the removal of abasic sites in yeast. Mol. Cell. Biol. 20: 3522-3528.
86. TRAN, H. T., N. P. DEGTYAREVA, N. N. KOLOTEVA, A. SUGINO, H. MASUMOTO et al., 1995 Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol. Cell. Biol. 15: 5607-5617.
87. TRAN, P. T., J. A. SIMON and R. M. LISKAY, 2001 Interactions of Exo1p with components of MutLα in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98: 9760-9765.
88. VAN SLOUN, P. P., I. VARLET, E. SONNEVELD, J. J. BOEI, R. J. ROMEIJN et al., 2002 Involvement of mouse Rev3 in tolerance of endogenous and exogenous DNA damage. Mol. Cell. Biol. 22: 2159-2169.
89. VENKATESAN, R. N., J. J. HSU, N. A. LAWRENCE, B. D. PRESTON and L. A. LOEB, 2006 Mutator phenotypes caused by substitution at a conserved motif A residue in eukaryotic DNA polymerase δ. J. Biol. Chem. 281: 4486-4494.
90. VON BORSTEL, R. C., R.W. ORD, S. P. STEWART, R.G. RITZEL, G. S. LEE et al., 1993 The mutator mut7-1 of Saccharomyces cerevisiae. Mutat. Res. 289: 97-106.
91. WACH, A., A. BRACHAT, R. POHLMANN and P. PHILIPPSEN, 1994 New heterologous modules for classical or PCR-based gene disruptions in S. cerevisiae. Yeast 10: 1793-1808.
92. WATERS, L. S., B. K. MINESINGER, M. E. WILTROUT, S. D'SOUZA, R. V. WOODRUFF et al., 2009 Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 73: 134-154.
93. WITTSCHIEBEN, J. P., S. C. RESHMI, S. M. GOLLIN and R. D. WOOD, 2006 Loss of DNA polymerase ζ causes chromosomal instability in mammalian cells. Cancer Res. 66: 134-142.
94. WOOD, A., P. GARG and P. M. BURGERS, 2007 A ubiquitin-binding motif in the translesion DNA polymerase Rev1 mediates its essential functional interaction with ubiquitinated proliferating cell nuclear antigen in response to DNA damage. J. Biol. Chem. 282: 20256-20263.
95. XIAO, W., B. L. CHOW, T. FONTANIE, L. MA, S. BACCHETTI et al., 1999 Genetic interactions between error-prone and error-free postreplication repair pathways in Saccharomyces cerevisiae. Mutat. Res. 435: 1-11.
96. XIAO, W., B. L. CHOW, M. HANNA, P. W. DOETSCH, Y. ZHU et al., 2001 Deletion of the MAG1 DNA glycosylase gene suppresses alkylation-induced killing and mutagenesis in yeast cells lacking AP endonucleases. Mutat. Res. 487: 137-147.
97. XIE, Z., Y. ZHANG, A. B. GULIAEV, H. SHEN, B. HANG et al., 2005 The p-benzoquinone DNA adducts derived from benzene are highly mutagenic. DNA Repair 4: 1399-1409.
98. YANG, Y., J. STERLING, F. STORICI, M. A. RESNICK and D. A. GORDENIN, 2008 Hypermutability of damaged single-strand DNA formed at double-strand breaks and uncapped telomeres in yeast Saccharomyces cerevisiae. PLoS Genet. 4: e1000264.
99. YU, S. L., S. K. LEE, R. E. JOHNSON, L. PRAKASH and S. PRAKASH, 2003 The stalling of transcription at abasic sites is highly mutagenic. Mol. Cell. Biol. 23: 382-388.
100. ZHAO, B., Z. XIE, H. SHEN and Z. WANG, 2004 Role of DNA polymerase η in the bypass of abasic sites in yeast cells. Nucleic Acids Res. 32: 3984-3994.
101. 2-dG DNA adducts in yeast cells. Nucleic Acids Res. 34: 417-425.
102. ZHONG, X., P. GARG, C. M. STITH, S. A. NICK MCELHINNY, G. E. KISSLING et al., 2006 The fidelity of DNA synthesis by yeast DNA polymerase ζ alone and with accessory proteins. Nucleic Acids Res. 34: 4731-4742.