Identification of a strand-related bias in the PCNA-mediated bypass of spontaneous lesions by yeast Polη

DNA Repair

Volumn 6, Issue 9, 2007, Pages 1307-1318

  Abdulovic, Amy L ^a   Minesinger, Brenda K ^a   Jinks Robertson, Sue ^a,b  

^a EMORY UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

PCNA; Pol ; Pol ; Translesion synthesis; Yeast

Indexed keywords

CYCLINE; DNA POLYMERASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL SURVIVAL; FRAMESHIFT MUTATION; GENE DUPLICATION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; ULTRAVIOLET RADIATION; WILD TYPE; YEAST;

BASE SEQUENCE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; DNA-DIRECTED DNA POLYMERASE; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; PROLIFERATING CELL NUCLEAR ANTIGEN; SACCHAROMYCES CEREVISIAE;

EID: 34547729196     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.02.026     Document Type: Article

References (64)

1. Rattray A.J., and Strathern J.N. Error-prone DNA polymerases: when making a mistake is the only way to get ahead. Annu. Rev. Genet. 37 (2003) 31-66
2. Ohmori H., Friedberg E.C., Fuchs R.P., Goodman M.F., Hanaoka F., Hinkle D., Kunkel T.A., Lawrence C.W., Livneh Z., Nohmi T., Prakash L., Prakash S., Todo T., Walker G.C., Wang Z., and Woodgate R. The Y-family of DNA polymerases. Mol. Cell 8 (2001) 7-8
3. Nelson J.R., Lawrence C.W., and Hinkle D.C. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 272 (1996) 1646-1649
4. Lawrence C.W. Cellular roles of DNA polymerase ζ and Rev1 protein. DNA Repair (Amst.) 1 (2002) 425-435
5. Johnson R.E., Yu S.L., Prakash S., and Prakash L. Yeast DNA polymerase ζ (zeta) is essential for error-free replication past thymine glycol. Genes Dev. 17 (2003) 77-87
6. Quah S.K., von Borstel R.C., and Hastings P.J. The origin of spontaneous mutation in Saccharomyces cerevisiae. Genetics 96 (1980) 819-839
7. Prakash S., and Prakash L. Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair. Genes Dev. 16 (2002) 1872-1883
8. Nelson J.R., Lawrence C.W., and Hinkle D.C. Deoxycytidyl transferase activity of yeast REV1 protein. Nature 382 (1996) 729-731
9. Haracska L., Prakash S., and Prakash L. Yeast Rev1 protein is a G template-specific DNA polymerase. J. Biol. Chem. 277 (2002) 15546-15551
10. Harfe B.D., and Jinks-Robertson S. DNA polymerase ζ introduces multiple mutations when bypassing spontaneous DNA damage in Saccharomyces cerevisiae. Mol. Cell 6 (2000) 1491-1499
11. Washington M.T., Minko I.G., Johnson R.E., Haracska L., Harris T.M., Lloyd R.S., Prakash S., and Prakash L. Efficient and error-free replication past a minor-groove N2-guanine adduct by the sequential action of yeast Rev1 and DNA polymerase ζ. Mol. Cell. Biol. 24 (2004) 6900-6906
12. Roush A.A., Suarez M., Friedberg E.C., Radman M., and Siede W. Deletion of the Saccharomyces cerevisiae gene RAD30 encoding an Escherichia coli DinB homolog confers UV radiation sensitivity and altered mutability. Mol. Gen. Genet. 257 (1998) 686-692
13. McDonald J.P., Levine A.S., and Woodgate R. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics 147 (1997) 1557-1568
14. Johnson R.E., Haracska L., Prakash S., and Prakash L. Role of DNA polymerase ζ in the bypass of a (6-4) TT photoproduct. Mol. Cell. Biol. 21 (2001) 3558-3563
15. Yuan F., Zhang Y., Rajpal D.K., Wu X., Guo D., Wang M., Taylor J.S., and Wang Z. Specificity of DNA lesion bypass by the yeast DNA polymerase η. J. Biol. Chem. 275 (2000) 8233-8239
16. Haracska L., Yu S.L., Johnson R.E., Prakash L., and Prakash S. Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase η. Nat. Genet. 25 (2000) 458-461
17. Johnson R.E., Prakash S., and Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Polη. Science 283 (1999) 1001-1004
18. Bresson A., and Fuchs R.P. Lesion bypass in yeast cells: Pol η participates in a multi-DNA polymerase process. EMBO J. 21 (2002) 3881-3887
19. Gibbs P.E., McDonald J., Woodgate R., and Lawrence C.W. 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 (2005) 575-582
20. Abdulovic A.L., and Jinks-Robertson S. The in vivo characterization of translesion synthesis across UV-induced lesions in Saccharomyces cerevisiae: insights into Polζ- and Polη-dependent frameshift mutagenesis. Genetics 172 (2006) 1487-1498
21. Kannouche P., and Stary A. Xeroderma pigmentosum variant and error-prone DNA polymerases. Biochimie 85 (2003) 1123-1132
22. Wittschieben J., Shivji M.K., Lalani E., Jacobs M.A., Marini F., Gearhart P.J., Rosewell I., Stamp G., and Wood R.D. Disruption of the developmentally regulated Rev3l gene causes embryonic lethality. Curr. Biol. 10 (2000) 1217-1220
23. Lehmann A.R., and Fuchs R.P. Gaps and forks in DNA replication: rediscovering old models. DNA Repair (Amst.) 5 (2006) 1495-1498
24. Veaute X., and Fuchs R.P. Greater susceptibility to mutations in lagging strand of DNA replication in Escherichia coli than in leading strand. Science 261 (1993) 598-600
25. Trinh T.Q., and Sinden R.R. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli. Nature 352 (1991) 544-547
26. Radman M. DNA replication: one strand may be more equal. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 9718-9719
27. Pavlov Y.I., Mian I.M., and Kunkel T.A. Evidence for preferential mismatch repair of lagging strand DNA replication errors in yeast. Curr. Biol. 13 (2003) 744-748
28. Gordenin D.A., Malkova A.L., Peterzen A., Kulikov V.N., Pavlov Y.I., Perkins E., and Resnick M.A. Transposon Tn5 excision in yeast: influence of DNA polymerases α, δ, and ε and repair genes. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 3785-3789
29. Pavlov Y.I., Newlon C.S., and Kunkel T.A. Yeast origins establish a strand bias for replicational mutagenesis. Mol. Cell 10 (2002) 207-213
30. Bambara R.A., Murante R.S., and Henricksen L.A. Enzymes and reactions at the eukaryotic DNA replication fork. J. Biol. Chem. 272 (1997) 4647-4650
31. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
32. Haracska L., Unk I., Prakash L., and Prakash S. Ubiquitylation of yeast proliferating cell nuclear antigen and its implications for translesion DNA synthesis. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 6477-6482
33. Stelter P., and Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425 (2003) 188-191
34. Garg P., Stith C.M., Majka J., and Burgers P.M. Proliferating cell nuclear antigen promotes translesion synthesis by DNA polymerase ζ. J. Biol. Chem. 280 (2005) 23446-23450
35. Haracska L., Kondratick C.M., Unk I., Prakash S., and Prakash L. Interaction with PCNA is essential for yeast DNA polymerase η function. Mol. Cell 8 (2001) 407-415
36. Plosky B.S., Vidal A.E., Fernandez de Henestrosa A.R., McLenigan M.P., McDonald J.P., Mead S., and Woodgate R. Controlling the subcellular localization of DNA polymerases ι and η via interactions with ubiquitin. EMBO J. 25 (2006) 2847-2855
37. Guo C., Sonoda E., Tang T.S., Parker J.L., Bielen A.B., Takeda S., Ulrich H.D., and Friedberg E.C. REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol. Cell 23 (2006) 265-271
38. Garg P., and Burgers P.M. Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases η and REV1. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 18361-18366
39. Sabbioneda S., Minesinger B.K., Giannattasio M., Plevani P., Muzi-Falconi M., and Jinks-Robertson S. The 9-1-1 checkpoint clamp physically interacts with Polζ and is partially required for spontaneous Polζ-dependent mutagenesis in Saccharomyces cerevisiae. J. Biol. Chem. 280 (2005) 38657-38665
40. Minesinger B.K., and Jinks-Robertson S. Roles of RAD6 epistasis group members in spontaneous Polζ-dependent translesion synthesis in Saccharomyces cerevisiae. Genetics 169 (2005) 1939-1955
41. Minesinger B.K., Abdulovic A.L., Ou T.M., and Jinks-Robertson S. The effect of oxidative metabolism on spontaneous Polζ-dependent translesion synthesis in Saccharomyces cerevisiae. DNA Repair (Amst.) 5 (2006) 226-234
42. Gietz R.D., Schiestl R.H., Willems A.R., and Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11 (1995) 355-360
43. Harfe B.D., and Jinks-Robertson S. Removal of frameshift intermediates by mismatch repair proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 19 (1999) 4766-4773
44. Storici F., Lewis L.K., and Resnick M.A. In vivo site-directed mutagenesis using oligonucleotides. Nat. Biotechnol. 19 (2001) 773-776
45. Wach A., Brachat A., Pohlmann R., and Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10 (1994) 1793-1808
46. Erdeniz N., Dudley S., Gealy R., Jinks-Robertson S., and Liskay R.M. Novel PMS1 alleles preferentially affect the repair of primer strand loops during DNA replication. Mol. Cell. Biol. 25 (2005) 9221-9231
47. Gueldener U., Heinisch J., Koehler G.J., Voss D., and Hegemann J.H. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30 (2002) e23
48. Deshpande A.M., and Newlon C.S. The ARS consensus sequence is required for chromosomal origin function in Saccharomyces cerevisiae. Mol. Cell. Biol. 12 (1992) 4305-4313
49. Goldstein A.L., and McCusker J.H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15 (1999) 1541-1553
50. lea D.E., and Coulson C.A. The distribution of the numbers of mutants in bacterial populations. J. Genet. 119 (1949) 264-284
51. Altman D.G. Practical Statistics for Medical Research (1990), CRC Press, New York
52. Spell R.M., and Jinks-Robertson S. Determination of mitotic recombination rates by fluctuation analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 262 (2004) 3-12
53. Hoffman C.S., and Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57 (1987) 267-272
54. Tran H.T., Degtyareva N.P., Koloteva N.N., Sugino A., Masumoto H., Gordenin D.A., and 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
55. Freudenreich C.H., Stavenhagen J.B., and Zakian V.A. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol. Cell. Biol. 17 (1997) 2090-2098
56. Carty M.P., Glynn M., Maher M., Smith T., Yao J., Dixon K., McCann J., Rynn L., and Flanagan A. The RAD30 cancer susceptibility gene. Biochem. Soc. Trans. 31 (2003) 252-256
57. Cordeiro-Stone M., Zaritskaya L.S., Price L.K., and Kaufmann W.K. Replication fork bypass of a pyrimidine dimer blocking leading strand DNA synthesis. J. Biol. Chem. 272 (1997) 13945-13954
58. McGregor W.G., Wei D., Maher V.M., and McCormick J.J. Abnormal, error-prone bypass of photoproducts by xeroderma pigmentosum variant cell extracts results in extreme strand bias for the kinds of mutations induced by UV light. Mol. Cell. Biol. 19 (1999) 147-154
59. Svoboda D.L., Briley L.P., and Vos J.M. Defective bypass replication of a leading strand cyclobutane thymine dimer in xeroderma pigmentosum variant cell extracts. Cancer Res. 58 (1998) 2445-2448
60. Theis J.F., Yang C., Schaefer C.B., and Newlon C.S. DNA sequence and functional analysis of homologous ARS elements of Saccharomyces cerevisiae and S. carlsbergensis. Genetics 152 (1999) 943-952
61. N. Kim, A.L. Abdulovic, R. Gealy, M.J. Lippert and S. Jinks-Robertson, Transcriptional-associated mutagenesis in yeast is directly proportional to the level of gene expression and influenced by the direction of DNA replication, DNA Repair (Amst.) (2007) (in press).
62. Lopes M., Foiani M., and Sogo J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21 (2006) 15-27
63. Woodgate R. Evolution of the two-step model for UV-mutagenesis. Mutat. Res. 485 (2001) 83-92
64. Zhong X., Garg P., Stith C.M., McElhinny S.A., Kissling G.E., Burgers P.M., and Kunkel T.A. The fidelity of DNA synthesis by yeast DNA polymerase zeta alone and with accessory proteins. Nucleic Acids Res. 34 (2006) 4731-4742