DNA polymerase ζ cooperates with polymerases κ and ι in translesion DNA synthesis across pyrimidine photodimers in cells from XPV patients

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 28, 2009, Pages 11552-11557

  Ziv, Omer ^a   Geacintov, Nicholas ^b   Nakajima, Satoshi ^c   Yasui, Akira ^c   Livneh, Zvi ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b NEW YORK UNIVERSITY   (United States)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

Carcinogenesis; DNA repair; Lesion bypass; Replication; Ultraviolet

Indexed keywords

DIMER; DNA POLYMERASE; DNA POLYMERASE IOTA; DNA POLYMERASE KAPPA; DNA POLYMERASE ZETA; PYRIMIDINE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA SYNTHESIS; EXCISION REPAIR; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; ULTRAVIOLET RADIATION; XERODERMA PIGMENTOSUM;

CELLS, CULTURED; DNA; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; HUMANS; MODELS, GENETIC; PYRIMIDINE DIMERS; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM;

EID: 67650928194     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0812548106     Document Type: Article

References (45)

1. Friedberg EC, et al. (2006) DNA Repair and Mutagenesis (ASM Press, Washington DC), 2nd edition.
2. Livneh Z (2001) DNA damage control by novel DNA polymerases: Translesion replication and mutagenesis. J Biol Chem 276:25639-25642.
3. Prakash S, Johnson RE, Prakash L (2005) Eukaryotic translesion synthesis DNA polymerases: Specificity of structure and function. Annu Rev Biochem 74:317-353.
4. Yang W, Woodgate R (2007) What a difference a decade makes: Insights into translesion synthesis. Proc Natl Acad Sci USA 104:15591-15598.
5. Gan GN, Wittschieben JP, Wittschieben BO, Wood RD (2008) DNA polymerase ζ (pol ζ) in higher eukaryotes. Cell Research 18:174-183.
6. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-141.
7. Kannouche PL, Wing J, Lehmann AR (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.
8. Avkin S, et al. (2006) p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol Cell 22:407-413.
9. Soria G, Podhajcer O, Gottifredi V (2006) P21Cip1/WAF1 downregulation is required for efficient PCNA ubiquitination after UV irradiation. Oncogene 25:2829-2838.
10. Masutani C, et al. (1999) The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399:700-704.
11. Johnson RE, Kondratick CM, Prakash S, Prakash L (1999) hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 285:263-265.
12. Maher VM, Ouellette LM, Curren RD, McCormick JJ (1976) Frequency of ultraviolet light-induced mutations is higher in xeroderma pigmentosum variant cells than in normal human cells. Nature 261:593-595.
13. Dumstorf CA, et al. (2006) Participation of mouse DNA polymerase ι in strand-biased mutagenic bypass of UV photoproducts and suppression of skin cancer. Proc Natl Acad Sci USA 103:18083-18088.
14. Wang Y, et al. (2007) Evidence that in xeroderma pigmentosum variant cells, which lack DNA polymerase η, DNA polymerase iota causes the very high frequency and unique spectrum of UV-induced mutations. Cancer Res 67:3018-3026.
15. Gueranger Q, et al. (2008) Role of human DNA polymerases η, ι, and ζ in UV resistance and UV-induced mutagenesis. DNA Repair 7:1551-1562.
16. Avkin S, et al. (2004) Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells. The Role of DNA polymerase k. J Biol Chem 279:53298-53305.
17. Shachar S, et al. (2009) Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J 28:383-393.
18. Lehmann AR, Fuchs RP (2006) Gaps and forks in DNA Replication: Rediscovering old models. DNA Repair 5:1595-1598.
19. Hendel A, Ziv O, Gueranger Q, Geacintov N, Livneh Z (2008) Reduced fidelity and increased efficiency of translesion DNA synthesis across a TT cyclobutane pyrimidine dimer, but not a TT 6-4 photoproduct, in human cells lacking DNA polymerase η. DNA Repair 7:1636-1646.
20. Johnson RE, Prakash S, Prakash L (1999) Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Pol η. Science 283:1001-1004.
21. Ohashi E, et al. (2000) Error-prone bypass of certain DNA lesions by the human DNA polymerase κ. Genes Dev 14:1589-1594.
22. Petta TB, et al. (2008) Human DNA polymerase ι protects cells against oxidative stress. EMBO J 27:2883-2895.
23. Ogi T, Lehmann AR (2006) The Y-family DNA polymerase κ (pol κ) functions in mammalian nucleotide-excision repair. Nat Cell Biol 8:640-642.
24. Nakajima S, et al. (2004) UV light-induced DNA damage and tolerance for the survival of nucleotide excision repair-deficient human cells. J Biol Chem 279:46674-46677.
25. Vaisman A, et al. (2003) Sequence context-dependent replication of DNA templates containing UV-induced lesions by human DNA polymerase ι. DNA Repair 2:991-1006.
26. Johnson RE, Washington MT, Haracska L, Prakash S, Prakash L (2000) Eukaryotic polymerases ι and ζ act sequentially to bypass DNA lesions. Nature 406:1015-1019.
27. Washington MT, Johnson RE, Prakash L, Prakash S (2002) Human DINB1-encoded DNA polymerase κ is a promiscuous extender of mispaired primer termini. Proc Natl Acad Sci USA 99:1910-1914.
28. Gibbs PE, McDonald J, Woodgate R, Lawrence CW (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 cyclobutyl dimer. Genetics 169:575-582.
29. Wittschieben JP, Reshmi SC, Gollin SM, Wood RD (2006) Loss of DNA polymerase zeta causes chromosomal instability in mammalian cells. Cancer Res 66:134-142.
30. Zander L, Bemark M (2004) Immortalized mouse cell lines that lack a functional Rev3 gene are hypersensitive to UV irradiation and cisplatin treatment. DNA Repair (Amsterdam) 3:743-752.
31. Sonoda E, et al. (2003) Multiple roles of Rev3, the catalytic subunit of pol ζ in maintaining genome stability in vertebrates. EMBO J 22:3188-3197.
32. Gibbs PE, McGregor WG, Maher VM, Nisson P, Lawrence CW (1998) A human homolog of the Saccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase zeta. Proc Natl Acad Sci USA 95:6876-6880.
33. Li Z, et al. (2002) hREV3 is essential for eror-prone translesion synthesis past UV or benzopyrene diol expoxide-induced DNA lesions in human fibroblasts. Mutat Res 510:71-80.
34. Diaz M, et al. (2003) Decreased Frequency and Highly Aberrant Spectrum of Ultraviolet-Induced Mutations in the hprt Gene of Mouse Fibroblasts Expressing Antisense RNA to DNA Polymerase ζ. Mol Cancer Res 1:836-847.
35. Choi JH, Besaratinia A, Lee DH, Leeb CS, Pfeifer GP (2006) The role of DNA polymerase ι in UV mutational spectra. Mutat Res 599:58-65.
36. Tang M, et al. (1999) UmuD′(2)C is an error-prone DNA polymerase, Escherichia coli pol V Proc Natl Acad Sci USA 96:8919-8924.
37. Reuven NB, Arad G, Maor-Shoshani A, Livneh Z (1999) The mutagenesis protein UmuC is a DNA polymerase activated by UmuD′, RecA and SSB, and specialized for translesion replication. J Biol Chem 274:31763-31766.
38. Ogi T, Shinkai Y, Tanaka K, Ohmori H (2002) Pol κ protects mammalian cells against the lethal and mutagenic effects of benzopyrene. Proc Natl Acad Sci USA 99:15548-15553.
39. Ling H, Boudsocq F, Plosky BS, Woodgate R, Yang W (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature 424:1083-1087.
40. Li Y, et al. (2004) Nucleotide insertion opposite a cis-syn thymine dimer by a replicative DNA polymerase from bacteriophage T7. Nat Struct Mol Biol 11:784-790.
41. Garinis GA, et al. (2005) Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UV-induced DNA breaks. EMBO J 24:3952-3962.
42. Rajao MA, et al. (2008) DNA polymerase κ from Trypanosoma cruzi localizes to the mitochondria, bypasses 8-oxoguanine, and performs DNA synthesis in a recombination intermediate. Mol Microbiol In press:
43. Kawamoto T, et al. (2005) Dual roles for DNA polymerase η in homologous DNA recombination and translesion DNA synthesis. Mol Cell 20:793-799.
44. McIlwraith MJ, et al. (2005) Human DNA polymerase η promotes DNA synthesis from strand invasion intermediates of homologous recombination. Mol Cell 20:783-792.
45. Tomer G, Livneh Z (1999) Analysis of unassisted translesion replication by the DNA polymerase III holoenzyme. Biochemistry 38:5948-5958.