The roles of the eukaryotic DNA polymerases in DNA repair synthesis

Mutation Research - DNA Repair

Volumn 384, Issue 3, 1997, Pages 157-167

  Budd, Martin E ^a   Campbell, Judith L ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE DELTA; DNA DIRECTED DNA POLYMERASE GAMMA; DNA POLYMERASE;

DNA REPAIR; EUKARYOTE; EXCISION REPAIR; NONHUMAN; PRIORITY JOURNAL; REVIEW; YEAST;

ANIMALS; DNA REPAIR; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; EUKARYOTIC CELLS; HUMANS;

EUKARYOTA;

EID: 0030825134     PISSN: 09218777     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0921-8777(97)00024-4     Document Type: Review

References (89)

1. E.C. Friedberg, W. Siede, A.J. Cooper, Cellular responses to DNA damage in yeast, in: J.R. Broach, J.R. Pringle, E.R. Jones (Eds.), The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis and Energetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1991, pp. 147-192.
2. E.C. Friedberg, G.C. Walker, W. Siede, DNA Repair and Mutagenesis, ASM Press, Washington, DC, 1995.
3. Orr-Weaver T.L., Szostak J.W., Rothstein R.J. Yeast transformation: a model system for the study of recombination. Proc. Natl. Acad. Sci. USA. 78:1981;6354-6358.
4. Wang T.S.-F. Eukaryotic DNA polymerases. Ann. Rev. Biochem. 60:1991;513-552.
5. Araki H., Ropp P.A., Johnson A.L., Johnston L.H., Morrison A., Sugino A. DNA polymerase II, the probable homolog of mammalian DNA polymerase ε, replicates chromosomal DNA in the yeast Saccharomyces cerevisiae. EMBO J. 11:1992;733-740.
6. Boulet A., Simon M., Faye G., Bauer G.A., Burgers P.M.J. Structure and function of the Saccharomyces cerevisiae CDC2 gene encoding the large subunit of DNA polymerase III. EMBO J. 8:1989;1849-1854.
7. Budd M.E., Campbell J.L. DNA polymerases δ and ε are required for chromosomal replication in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:1993;496-505.
8. Budd M.E., Wittrup K.D., Bailey J.E., Campbell J.L. DNA polymerase I is required for DNA replication but not for repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 9:1989;365-376.
9. Budd M., Campbell J.L. Temperature sensitive mutants of yeast DNA polymerase I. Proc. Natl. Acad. Sci. USA. 84:1987;2838-2842.
10. Lucchini G., Falcolni M.M., Pizzagalli A., Aguilera A., Klein H.L., Plevani P. Nucleotide sequence and characterization of temperature-sensitive pol1 mutants of Saccharomyces cerevisiae. Gene. 90:1990;99-104.
11. Morrison A., Araki H., Clark A.B., Hamatake R.K., Sugino A. A third essential DNA polymerase in S. cerevisiae. Cell. 62:1990;1143-1151.
12. Sitney K.C., Budd M.E., Campbell J.L. DNA polymerase III, a second essential DNA polymerase, is encoded by the Saccharomyces cerevisiae. Cell. 56:1989;599-605.
13. Tsurimoto T., Stillman B. Functions of replication factor C and proliferating-cell nuclear antigen: functional similarity of DNA polymerase accessory proteins from human cells and bacteriophage T4. Proc. Natl. Acad. Sci. USA. 87:1990;1023-1027.
14. Bravo R., Frank R., Blundell P.A., Macdonald-Bravo H. Cyclin/PCNA is the auxiliary protein of DNA polymerase-δ Nature. 326:1987;515-517.
15. Prelich G., Tan C.-K., Kostura M., Mathews M.B., So A.G., Downey K.M., Stillman B. Functional identity of proliferating cell nuclear antigen and a DNA polymerase δ auxiliary protein. Nature. 326:1987;517-520.
16. Nethanel T., Kaufman G. Two DNA polymerases may be required for synthesis of the lagging DNA strand of simian virus 40. J. Virol. 64:1990;5912-5918.
17. Foury F. Cloning and sequencing of the nuclear gene MIP1 encoding the catalytic subunit of the yeast mitochondrial DNA polymerase. J. Biol. Chem. 264:1989;20552-20560.
18. Harris P.V., Mazina O.M., Leonhardt E.A., Case R.B., Boyd J.B. Molecular-cloning of Drosophila mus308. A gene involved in DNA cross-link repair with homology to prokaryotic DNA-polymerase-I genes. Mol. Cell. Biol. 16:1996;5764-5771.
19. Sugino A. Yeast DNA polyemrases and their role at the replication fork. Trends Biochem. 20:1995;319-323.
20. Budd M.E., Sitney K., Campbell J.L. Purification of DNA polymerase II, a distinct polymerase, from Saccharomyces cerevisiae. J. Biol. Chem. 264:1989;6557-6565.
21. Dresler S.L., Frattini M.G. DNA replication and UV-induced repair synthesis in human fibroblasts are much less sensitive than DNA polymerase α to inhibition by butylphenyl deoxy triphosphate. Fed. Proc. 46:1986;2208.
22. Dresler S.L., Gowans B.J., Robinson-Hill R.M., Hunting D.J. Involvement of DNA polymerase δ in DNA repair synthesis in human fibroblasts at late times after ultraviolet irradiation. Biochemistry. 27:1988;6379-6383.
23. Hammond R.A., McClung J.K., Miller M.R. Effect of DNA polymerase inhibitors on DNA repair in intact and permeable human fibroblasts: Evidence that DNA polymerases δ and β are involved in DNA repair synthesis induced by N-Methyl-N′-nitro-N-nitrosoguanidine. Biochemistry. 29:1990;286-291.
24. Oda N., Levin J.D., Spoonde A.Y., Frank E.G., Levine A.S., Woodgate R., Ackerman E.J. Arrested DNA replication in Xenopus and release by Escherichia coli mutagenesis proteins. Science. 272:1996;1644-1646.
25. Nishida C., Reinhard P., Linn S. DNA repair synthesis in human fibroblasts requires DNA polymerase δ J. Biol. Chem. 263:1988;501-510.
26. Wood R.D., Robins P., Lindahl T. Complementation of the Xeroderma pigmentosum DNA repair defect in cell-free extracts. Cell. 53:1988;97-106.
27. Shivji M.K.K., Kenny M.K., Wood R.D. Proliferating cell nuclear antigen is required for DNA excision repair. Cell. 69:1992;367-374.
28. Lee S.-H., Pan Z.-Q., Kwong A.D. Synthesis of DNA by DNA polymerase ε in vitro. J. Biol. Chem. 266:1991;22707-22717.
29. Ayyagari R., Impellizzeri K.J., Yoder B.L., Gary S.L., Burgers P.M.J. A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replciation and DNA repair. Mol. Cell. Biol. 15:1995;4420-4429.
30. Amin N.S., Holm C. In vivo anlaysis reveals that the interdomain region of the yeast proliferating cell nuclear antigen is important for DNA replication and DNA repair. Genetics. 144:1996;479-493.
31. Shivji M.K.K., Podust V.N., Hübscher U., Wood R.D. Nucleotide excision repair DNA synthesis by DNA polymerase ε in the presence of PCNA, RFC and RPA. Biochemistry. 34:1995;5011-5017.
32. Tsurimoto T., Stillman B. Replication factors required for SV40 DNA replication in vitro. II. Switching of DNA polymerase α and δ during initiation of leading and lagging strand synthesis. J. Biol. Chem. 266:1991;1961-1968.
33. Zeng X.R., Jiang Y., Zhang S.J., Hao H., Lee M.Y.W.T. DNA polymerase β is involved in the cellular response to UV damage in human cells. J. Biol. Chem. 269:1994;13748-13751.
34. Shivji, Wood, Which DNA polymerases are used for DNA repair in eukaryotes? Carcinogenesis (1997), in press.
35. Budd M.E., Campbell J.L. DNA polymerases required for repair of UV-induced damage in yeast. Mol. Cell. Biol. 15:1995;2173-2179.
36. Wilcox D.R., Prakash L. Incision and post-incision steps of pyrimidine dimer removal in excision defective mutants of Saccharomyces cerevisiae. J. Bacteriol. 148:1981;618-623.
37. Navas T.A., Zhou Z., Elledge S.J. DNA polymerase ε links the DNA replication machinery to the S phase checkpoint. Cell. 80:1995;29-39.
38. Johnson R.E., Kovvali G.K., Guzder S.N., Amin N.S., Holm C. Evidence for involvement of yeast proliferating cell nuclear antigen in DNA mismatch repair. J. Biol. Chem. 271:1996;27987-27990.
39. Umar A., Buermeyer A.B., Simon J.A., Thomas D.C., Clark A.B., Liskay R.M., Kunkel T.A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell. 87:1996;65-73.
40. Johnson R.E., Gopala K.K., Prakash L., Prakash S. Requirement for the yeast RTH1 5′ to 3′ exonuclease for the stability of simple repetitive DNA. Science. 269:1995;238-240.
41. Li X., Li J., Harrington J., Lieber M.R., Burgers P.M.J. Lagging strand DNA synthesis at the eukaryotic replication fork involves binding and stimulation of FEN-1 by proliferating cell nuclear antigen. J. Biol. Chem. 270:1995;22109-22112.
42. Reagan M.S., Pittenger C., Siede W., Friedberg E.C. Characterization of a mutant strain of Saccharomyces cerevisiae with a deletion of the RAD27 gene, a structural homolog of the RAD2 nucleotide excision-repair gene. J. Bacteriol. 177:1995;364-371.
43. Waga S., Bauer G., Stillman B. Reconstitution of complete SV40 DNA replication with purified replication factors. J. Biol. Chem. 269:1994;10923-10934.
44. Chen J.J., Chen S., Saha P., Dutta A. p21 (CIP1, WAF1) disrupts the recruitment of human FEN1 by proliferating cell nuclear antigen into the DNA replication complex. Proc. Natl. Acad. Sci. USA. 93:1996;11597-11602.
45. Torresramos C.A., Yoder B.L., Burgers P.M.J., Prakash S., Prakash L. Requirement of proliferating cell nuclear antigen in rad6-dependent postreplicational DNA-repair. PNAS. 93:1996;9676-9681.
46. Li R., Waga S., Hannon G.J., Beach D., Stillman B. Differnential effects by the p21 cdk inhibitor on PCNA-dependent DNA replication and repair. Nature. 371:1994;534-537.
47. Shivji M.K.K., Grey S.J., Strausfeld U.P., Wood R.D., Blow J.J. CIP1 inhibits DNA replication but not PCNA dependent nucleotide excision repair. Curr. Biol. 4:1994;1062-1068.
48. Waga S., Hannon G.J., Beach D., Stillman B. The p21 inhibitor of cyclin-dependent kinases controls DNA-replication by interaction with PCNA. Nature. 369:1994;574-578.
49. Nealon K., Nicholl I.D., Kenny M.K. Characterization of the DNA polymerase requirement of human base excision repair. Nucleic Acids Res. 24(19):1996;3763-3770.
50. Matsumoto Y., Kim K., Bogenhagen D.F. Proliferating cell nuclear antigen-dependent abasic site repair in Xenopus laevis oocytes - an alternative pathway of base excision DNA repair. Mol. Cell. Biol. 14:1994;6187-6197.
51. Wang Z., Wu X., Friedberg E.C. DNA repair synthesis during base excision repair in vitro is catalyzed by DNA polymerase ε and is influenced by DNA polymerases α and β in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:1993;1051-1058.
52. Blank A., Kim B., Loeb L. DNA polymerase δ is required for base excision repair of DNA methylation damage in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 91:1994;9047-9051.
53. Suszek W., Baranowska H., Zuk J., Jachymczyk W.J. DNA polymerase III is required for DNA repair in Saccharomyces cerevisiae. Curr. Genet. 24:1993;200-204.
54. Paulovich A.G., Hartwell L.H. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell. 82:1995;841-847.
55. Gordenin D.A., Lobachev K.S., Degtyareva N.P., Malkova A.L., Perkins E., Resnick M.A. Inverted DNA repeats: a source of eukaryotic genomic instability. Mol. Cell. Biol. 13(9):1993;5315-5322.
56. Gordenin D.A., Malkova A.L., Peterzen A., Kulikov Y.I., Pavlov Y.I. Transposon Tn5 excision in yeast; the influence of DNA polymerase α, ε and repair genes. Proc. Natl. Acad. Sci. USA. 89:1992;3785-3789.
57. H. Tran, J.D. Keen, M.A. Kricker, M.A. Resnick, D.A. Gordenin, Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants, Mol. Cell. Biol. 15 (1997), in press.
58. Tran H.T., Degtyareva N.P., Kolotevea N.N., Sugino A., Matsumoto H., Gordenin D.A., Resnick M.A. Replication slippage between distant short repeats in saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol. Cell. Biol. 15:1995;5607-5617.
59. Tran H.T., Gordenin D.A., Resnick M.A. The prevention of repeat-associated deletions in saccharomyces cerevisiae by mismatch repair depends on size and origin of deletions. Genetics. 143:1996;1579-1587.
60. Dacosta L.T., Liu B., Eldeiry W.S., Hamilton S.R., Kinzler K.W., Vogelstein B., Markowitz S., Willson J.K.V., Delachapelle A.et al. Polymerase delta variants in RER colorectal tumors. Nat. Genet. 9:1995;10-11.
61. Fabre F., Boulet A., Faye G. Possible involvement of the yeast POLIII DNA polymrase in induced gene conversion. Mol. Gen. Genet. 229:1991;353-356.
62. Jessberger R., Chui G., Linn S., Kemper B. Analysis of the mammalian recombination protein complex RC-1. Mutagenesis. 350:1996;217-227.
63. M.E. Budd, J.L. Campbell, Identification of a new yeast DNA polymerase of the DNA polymerase β family and evidence supporting a role in meiosis, J. Biol. Chem. (1995).
64. Prasad R., Widen S.G., Singhal R.K., Watkins J., Prakash L., Wilson S.H. Yeast open reading frame YCR14C encodes a DNA β polymerase-like enzyme. Nucleic Acids Res. 21:1993;5301-5307.
65. Shimizu K., Sugino A. Purification and characterization of DNA helicase III from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 268:1993;9578-9584.
66. Dianov G., Lindahl T. Reconstitution of the DNA base excision-repair pathway. Curr. Biol. 4:1994;1069-1076.
67. Dianov G., Price A., Lindahl T. Generation of single-nucleotide repair patches following excision of uracil residues from DNA. Mol. Cell. Biol. 12:1992;1605-1612.
68. Singhal R.K., Prasad R., Wilson S.H. DNA polymerase β conducts the gap filling step in uracil initiated base excision repair in a bovine testis nuclear extract. J. Biol. Chem. 270:1995;949-957.
69. Wiebauer K., Jiricny J. Mismatch-specific thymine DNA glycosylase and DNA polymerase β mediate the correction of G:T mispairs in nuclear extracts from human cells. Proc. Natl. Acad. Sci. USA. 87:1990;5842-5845.
70. Matsumoto Y., Bogenhagen D.F. Repair of a synthetic abasic site in DNA in a Xenopus laevis oocyte extract. Mol. Cell. Biol. 9:1989;3750-3757.
71. Matsumoto Y., Kim K. Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair. Science. 269:1995;699-702.
72. Gu H., Marth J.D., Orban P.C., Mossmann H., Rajewsky K. Deletion of a DNA polymerase β gene segment in T-cells using cell-type-specific gene targeting. Science. 265:1994;103-106.
73. Sobol R.W., Horton J.K., Kuhn R., Gu H., Singhal R.K., Prasad R., Rajewsky K., Wilson S.H. Requirement of mammalian DNA polymerase β in base-excision repair. Nature. 379:1996;183-186.
74. Pelletier H., Sawaya M.R., Wolfle W., Wilson S.H., Kraut J. Crystal structures of human DNA polymerase β complexed with DNA-implications for catalytic mechanism processivity and fidelity. Biochemistry. 35:1996;12742-12761.
75. Piersen C.E., Prasad R., Wilson S.H., Lloyd R.H. Evidence for an imino intermediate in the DNA polymerase β deoxyribose phosphate excision reaction. J. Biol. Chem. 271:1996;17811-17815.
76. Mosbaugh D.W., Linn S. Excision repair and DNA synthesis with a combination of Hela DNA polymerase β and DNase V. J. Biol. Chem. 258:1983;108-118.
77. Caldecott K.W., Aoufouchi S., Johnson P., Shall S. XRCC1 polypeptide interacts with DNA polymerase β and possibly poly (ADP-ribose) polymerase and DNA ligase III is a novel molecular 'nicksensor' in vitro. Nucleic Acids Res. 24:1996;4387-4394.
78. Thompson L.H., Brookman K.W., Dillehay L.E., Carrano A.V., Mazrimas J.A., Mooney C.L., Minkler J.L. A CHO-cell strain having hypersensitivity to mutagens, a defect in strand-break repair and an extraordinarily baseline frequency of sister chromatid exchange. Mut. Res. 95:1982;427-440.
79. Prasad R., Singhal R.K., Srivastava K., Molina J.T., Tomkinson A.E., Wilson S.H. Specific interaction of DNA polymerase β and DNA ligase I in a multiprotein base excision repair complex from bovine testis. J. Biol. Chem. 271:1996;16000-16007.
80. Wang L., Patel U., Ghosh L., Banerjee S. DNA polymerase β mutations in human colorectal cancer. Cancer Res. 52:1992;4824-4827.
81. Scherbakova P.V., Pavlov Y.I. 3′-5′ exonucleases of DNA polymerases ε and δ correct base analog induced DNA replication errors on opposite DNA strands in Saccharomyces cerevisiae. Genetics. 142:1996;717-726.
82. J.R. Nelson, C.W. Lawrence, D.C. Hinkle, Thymine-thymine dimer bypass by yeast DNA polymerase ζ, 272 (1996) 1646-1648.
83. O'Day C.L. PCNA-induced DNA synthesis past cys-syn I thymine dimers by calf thymus DNA polymerase δ in vitro. Nucleic Acids Res. 20:1992;5403-5406.
84. Lawrence C. Teh Rad6 DNA repair pathway in Saccharomyces cerevisiae. Bioessays. 19:1993;253-258.
85. Strauss B.S. The A-rule of mutagen specificity-A consequence of DNA polymerase bypass of non-instructional lesions. Bioessays. 13:1991;79-84.
86. Ehmann U.K., Cook K.H., Friedberg E.C. The kinetics of thymine dimer excision in ultraviolet-irradiated human cells. Biophys. J. 22:1978;249-264.
87. Cox B., Game J. Repair systems in Saccharomyces. Mutat. Res. 26:1974;257-264.
88. Glassner B.J., Mortimer R.K. Synergistic interactions between RAD5, RAD16 and RAD54, three partially homologous yeast DNA repair genes each in a different repair pathway. Radiat. Res. 139:1994;24-33.
89. Resnick M., Martin P. The repair of double stranded breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol. Gen. Genet. 143:1976;112-129.