DNA sequence context greatly affects the accuracy of bypass across an ultraviolet light 6-4 photoproduct in mammalian cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 780, Issue , 2015, Pages 71-76

  Shriber, Pola ^a   Leitner Dagan, Yael ^a   Geacintov, Nicholas ^b   Paz Elizur, Tamar ^a   Livneh, Zvi ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

DNA damage; DNA repair; Error prone repair; Lesion bypass; UV mutagenesis

Indexed keywords

PYRIMIDINE DIMER; PYRIMIDINONE DERIVATIVE; THYMINE DERIVATIVE; THYMINE THYMINE PYRIMIDINE PYRIMIDONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA FLANKING REGION; DNA SEQUENCE; DNA SYNTHESIS; EMBRYO; FETUS; HUMAN; HUMAN CELL; MAMMAL CELL; MEASUREMENT ACCURACY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; TRANSLESION DNA SYNTHESIS; ULTRAVIOLET RADIATION; ADVERSE EFFECTS; ANIMAL; GENETICS; METABOLISM; MUTATION; SPECIES DIFFERENCE; TRANSFORMED CELL LINE;

MAMMALIA;

ANIMALS; CELL LINE, TRANSFORMED; DNA DAMAGE; HUMANS; MICE; MUTATION; PYRIMIDINE DIMERS; SPECIES SPECIFICITY; ULTRAVIOLET RAYS;

EID: 84940044140     PISSN: 00275107     EISSN: 18792871     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2015.08.002     Document Type: Article

References (37)

1. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington DC. 2nd edition.
2. Lehmann A.R., Fuchs R.P. Gaps and forks in DNA replication: rediscovering old models. DNA Repair 2006, 5:1498-1595.
3. Friedberg E.C. Suffering in silence: the tolerance of DNA damage. Nat. Rev. Mol. Cell Biol. 2005, 6:943-953.
4. Livneh Z., Cohen-Fix O., Skaliter R., Elizur T. Replication of damaged DNA and the molecular mechanism of ultraviolet light mutagenesis. CRC Crit. Rev. Biochem. Mol. Biol. 1993, 28:465-513.
5. Livneh Z., Ziv O., Shachar S. Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis. Cell Cycle 2010, 9:729-735.
6. Sale J.E., Lehmann A.R., Woodgate R. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol. 2012, 13:141-152.
7. Zhang H., Lawrence C.W. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15954-15959.
8. Berdichevsky A., Izhar L., Livneh Z. Error-free recombinational repair predominates over mutagenic translesion replication in E. coli. Mol. Cell 2002, 10:917-924.
9. Izhar L., Ziv O., Cohen I.S., Geacintov N., Livneh Z. Genomic assay reveals tolerance of DNA damage by both translesion DNA synthesis and homology-dependent repair in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E1462-E1469.
10. Cohen I.S., Bar C., Paz-Elizur T., Ainbinder E., Leopold K., de Wind N., Geacintov N., Livneh Z. DNA lesion identity drives choice of damage tolerance pathway in murine cell chromosomes. Nucl. Acids Res. 2015, 43:1637-1645.
11. Masutani C., Kusumoto R., Yamada A., Dohmae N., Yokoi M., Yuasa M., Araki M., Iwai S., Takio K., Hanaoka F. The XPV (xeroderma pigmentosum variant) gene encodes human DNA polymerase eta. Nature 1999, 399:700-704.
12. Johnson R.E., Kondratick C.M., Prakash S., Prakash L. hRAD30 mutations in the variant form of xeroderma pigmentosum. Science 1999, 285:263-265.
13. Shachar S., Ziv O., Avkin S., Adar S., Wittschieben J., Reissner T., Chaney S., Friedberg E.C., Wang Z., Carell T., et al. Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J. 2009, 28:383-393.
14. Vreeswijk M.P., van Hoffen A., Westland B.E., Vrieling H., van Zeeland A.A., Mullenders L.H. Analysis of repair of cyclobutane pyrimidine dimers and pyrimidine 6-4 pyrimidone photoproducts in transcriptionally active and inactive genes in Chinese hamster cells. J. Biol. Chem. 1994, 269:31858-31863.
15. Tung B.S., McGregor W.G., Wang Y.C., Maher V.M., McCormick J.J. Comparison of the rate of excision of major UV photoproducts in the human HPRT gene of normal and xeroderma pigmentosum variant cells. Mutat. Res. 1996, 362:65-74.
16. Nakajima S., Lan L., Kanno S., Takao M., Yamamoto K., Eker A.P., Yasui A. UV light-induced DNA damage and tolerance for the survival of nucleotide excision repair-deficient human cells. J. Biol. Chem. 2004, 279:46674-46677.
17. LeClerc J.E., Borden A., Lawrence C.W. The thymine-thymine pyrimidine-pyrimidone(6-4) ultraviolet light photoproduct is highly mutagenic and specifically induces 3' thymine-to-cytosine transitions in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:9685-9689.
18. Gentil A., Le Page F., Margot A., Lawrence C.W., Borden A., Sarasin A. Mutagenicity of a unique thymine-thymine dimer or thymine-thymine pyrimidine-pyrimidone (6-4) photoproduct in mammalian cells. Nucl. Acids Res. 1996, 24:1837-1840.
19. Hendel A., Ziv O., Gueranger Q., Geacintov N., Livneh Z. 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 eta. DNA Repair 2008, 7:1636-1646.
20. Yoon J.H., Prakash L., Prakash S. Error-free replicative bypass of (6-4) photoproducts by DNA polymerase zeta in mouse and human cells. Genes Dev. 2010, 24:123-128.
21. Reuven N.B., Arad G., Stasiak A.Z., Stasiak A., Livneh Z. Lesion bypass by the Escherichia coli DNA polymerase V requires assembly of a RecA nucleoprotein filament. J. Biol. Chem. 2001, 276:5511-5517.
22. Hendel A., Krijger P.H., Diamant N., Goren Z., Langerak P., Kim J., Reissner T., Lee K.Y., Geacintov N.E., Carell T., et al. PCNA ubiquitination is important, but not essential for translesion DNA synthesis in mammalian cells. PLoS Genet. 2011, 7:e1002262.
23. Ziv O., Diamant N., Shachar S., Hendel A., Livneh Z. Quantitative measurement of translesion DNA synthesis in mammalian cells. Methods Mol. Biol. 2012, 920:529-542.
24. Avkin S., Adar S., Blander G., Livneh Z. Quantitative measurement of translesion replication in human cells: evidence for bypass of abasic sites by a replicative DNA polymerase. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3764-3769.
25. Avkin S., Sevilya Z., Toube L., Geacintov N.E., Chaney S.G., Oren M., Livneh Z. p53 and p21 regulate error-prone DNA repair to yield a lower mutation load. Mol. Cell 2006, 22:407-413.
26. Diamant N., Hendel A., Vered I., Carell T., Reissner T., de Wind N., Geacintov N., Livneh Z. DNA damage bypass operates in the S and G2 phases of the cell cycle and exhibits differential mutagenicity. Nucl. Acids Res. 2012, 40:170-180.
27. Ziv O., Zeisel A., Mirlas-Neisberg N., Swain U., Nevo R., Ben-Chetrit N., Martelli M.P., Rossi R., Schiesser S., Canman C.E., et al. Identification of novel DNA-damage tolerance genes reveals regulation of translesion DNA synthesis by nucleophosmin. Nat. Commun. 2014, 5:5437.
28. Avkin S., Goldsmith M., Velasco-Miguel S., Geacintov N., Friedberg E.C., Livneh Z. Quantitative analysis of translesion DNA synthesis across a benzo[a]pyrene-guanine adduct in mammalian cells. The role of DNA polymerase κ. J. Biol. Chem. 2004, 279:53298-53305.
29. Gan G.N., Wittschieben J.P., Wittschieben B.O., Wood R.D. DNA polymerase zeta (pol zeta) in higher eukaryotes. Cell Res. 2008, 18:174-183.
30. Paz-Elizur T., Takeshita M., Goodman M., O'Donnell M., Livneh Z. Mechanism of translesion DNA synthesis by DNA polymerase II: comparison to DNA polymerases I and II. J. Biol. Chem. 1996, 271:24662-24669.
31. Daube S.S., Arad G., Livneh Z. Translesion replication by DNA polymerase beta is modulated by sequence context and stimulated by fork-like flap structures in DNA. Biochemistry 2000, 39:397-405.
32. Maccabee M., Evans J.S., Glackin M.P., Hatahet Z., Wallace S.S. Pyrimidine ring fragmentation products. Effects of lesion structure and sequence context on mutagenesis. J. Mol. Biol. 1994, 236:514-530.
33. Belguise V.P., Fuchs R.P. N-2-aminofluorene and N-2 acetylaminofluorene adducts: the local sequence context of an adduct and its chemical structure determine its replication properties. J. Mol. Biol. 1995, 249:903-913.
34. Moriya M., Spiegel S., Fernandes A., Amin S., Liu T., Geacintov N., Grollman A.P. Fidelity of translesional synthesis past benzo[a]pyrene diol epoxide-2'-deoxyguanosine DNA adducts: marked effects of host cell, sequence context, and chirality. Biochemistry 1996, 35:16646-16651.
35. Stone J.E., Kumar D., Binz S.K., Inase A., Iwai S., Chabes A., Burgers P.M., Kunkel T.A. Lesion bypass by S. cerevisiae Pol zeta alone. DNA Repair (Amst.) 2011, 10:826-834.
36. Jansen J.G., Temviriyanukul P., Wit N., Delbos F., Reynaud C.A., Jacobs H., de Wind N. Redundancy of mammalian Y family DNA polymerases in cellular responses to genomic DNA lesions induced by ultraviolet light. Nucl. Acids Res. 2014, 42:11071-11082.
37. Cai Y., Patel D.J., Broyde S., Geacintov N.E. Base sequence context effects on nucleotide excision repair. J. Nucl. Acids 2010, 9. Article ID. 10.4061/2010/174252.