Nucleotide Incision Repair: An Alternative and Ubiquitous Pathway to Handle Oxidative DNA Damage

  • Sophie Couvé-Privat
  • Alexander A. Ishchenko
  • Jacques Laval
  • Murat Saparbaev
Part of the Molecular Biology Intelligence Unit book series (MBIU)


Aerobic respiration and exogenous factors such as ionizing radiation and drugs generate reactive oxygen species (ROS). DNA has limited chemical stability and it is one of the most biologically important targets of ROS.1 Oxidative DNA lesions are believed to be a major type of endogenous damage leading to human degenerative disorders including cancer, cardiovascular disease and brain dysfunction. The clinical features of inherited human DNA repair deficiency disorders such as Cockayne syndrome and Fanconi’s anemia point to the complex nature of endogenous oxidative DNA damage which may include bulky adducts, interstrand crosslinks and clustered lesions. Oxidized DNA bases are substrates for two overlapping pathways: base excision repair (BER) and nucleotide incision repair (NIR). In the BER pathway, a DNA glycosylase clealvles the N-glycosylic bond between the modified base and deoxyribose, leaving either an abasic site or a single-strand break in DNA.2 Alternatively, in the NIR pathway, an apurinic/apyrimidinic (AP) endonuclease incises oxidatively damage DNA in a DNA glycosylase-independent manner, providing the correct ends for DNA synthesis, coupled to the repair of the remaining 5′-dangling modified nucleotide.3 We have demonstrated that the major human apurinic/apyrimidinic (AP) endonuclease (Ape1) is involved in the NIR pathway.4 NIR and BER pathways share many common substrates suggesting that they work in concert to cleanse genomic DNA of potentially mutagenic and cytotoxic lesions. Recently, we have genetically separated AP endonuclease and nucleotide incision activities to demonstrate that NIR handles a distinct type of oxidative DNA damage that cannot be processed in the BER pathway.5 The aim of this review is to summarise the present knowledge about the alternative DNA repair pathways for oxidised base modifications.


Proliferate Cell Nuclear Antigen Base Excision Repair Exonuclease Activity Abasic Site Base Excision Repair Pathway 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993; 362:709–715.PubMedCrossRefGoogle Scholar
  2. 2.
    Barnes DE, Lindahl T. Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu Rev Genet 2004; 38:445–476.PubMedCrossRefGoogle Scholar
  3. 3.
    Ischenko AA, Saparbaev MK. Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature 2002; 415:183–187.PubMedCrossRefGoogle Scholar
  4. 4.
    Gros L, Ishchenko AA, Ide H et al. The major human AP endonuclease (Ape1) is involved in the nucleotide incision repair pathway. Nucleic Acids Res 2004; 32:73–81.PubMedCrossRefGoogle Scholar
  5. 5.
    Ishchenko AA, Deprez E, Maksimenko A et al. Uncoupling of the base excision and nucleotide incision repair pathways reveals their respective biological roles. Proc Natl Acad Sci USA 2006; 103:2564–2569.PubMedCrossRefGoogle Scholar
  6. 6.
    Friedberg EC, Meira LB. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair (Amst) 2006; 5:189–209.CrossRefGoogle Scholar
  7. 7.
    Lindahl T. Two enzymes are required from strand incision in repair of alkylated DNA. Nature 1977; 269:829–832.CrossRefGoogle Scholar
  8. 9.
    Cunningham RP, Weiss B. Endonuclease III (nth) mutants of Escherichia coli. Proc Natl Acad Sci USA 1985; 82:474–478.PubMedCrossRefGoogle Scholar
  9. 10.
    Blaisdell JO, Wallace SS. Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. Proc Natl Acad Sci USA 2001; 98:7426–7430.PubMedCrossRefGoogle Scholar
  10. 11.
    Thomas D, Scot AD, Barbey R et al. Inactivation of OGG1 increases the incidence of G.C→T. A transversions in Saccharomyces cerevisiae: Evidence for endogenous oxidative damage to DNA in eukaryotic cells. Mol Gen Genet 1997; 254:171–178.PubMedCrossRefGoogle Scholar
  11. 12.
    Alseth I, Eide L, Pirovano M et al. The Saccharomyces cerevisiae homologues of endonuclease III from Escherichia coli, Ntg1 and Ntg2, are both required for efficient repair of spontaneous and induced oxidative DNA damage in yeast. Mol Cell Biol 1999; 19:3779–3787.PubMedGoogle Scholar
  12. 13.
    Saito Y, Uraki F, Nakajima S et al. Characterization of endonuclease III (nth) and endonuclease VIII (nei) mutants of Escherichia coli K-12. J Bacteriol 1997; 179:3783–3785.PubMedGoogle Scholar
  13. 14.
    Rosenquist TA, Zaika E, Fernandes AS et al. The novel DNA glycosylase, NEIL1, protects mammalian cells from radiation-mediated cell death. DNA Repair (Amst) 2003; 2:581–591.CrossRefGoogle Scholar
  14. 15.
    Eide L, Bjoras M, Pirovano M et al. Base excision of oxidative purine and pyrimidine DNA damage in Saccharomyces cerevisiae by a DNA glycosylase with sequence similarity to endonuclease III from Escherichia coli. Proc Natl Acad Sci USA 1996; 93:10735–10740.PubMedCrossRefGoogle Scholar
  15. 16.
    Karahalil B, de Souza-Pinto NC, Parsons JL et al. Compromised incision of oxidized pyrimidines in liver mitochondria of mice deficient in NTH1 and OGG1 glycosylases. J Biol Chem 2003; 278:33701–33707.PubMedCrossRefGoogle Scholar
  16. 17.
    Parsons JL, Elder RH. DNA N-glycosylase deficient mice: A tale of redundancy. Mutat Res 2003; 531:165–175.PubMedGoogle Scholar
  17. 18.
    Cunningham RP, Saporito SM, Spitzer SG et al. Endonuclease IV (nfo) mutant of Escherichia coli. J Bacteriol 1986; 168:1120–1127.PubMedGoogle Scholar
  18. 19.
    Ludwig DL, MacInnes MA, Takiguchi Y et al. A murine AP-endonuclease gene-targeted deficiency with post-implantation embryonic progression and ionizing radiation sensitivity. Mutat Res 1998; 409:17–29.PubMedGoogle Scholar
  19. 20.
    Bennett RA. The Saccharomyces cerevisiae ETH1 gene, and inducible homolog of exonuclease III that provides resistance to DNA-damaging agents and limits spontaneous mutagenesis. Mol Cell Biol 1999; 19:1800–1809.PubMedGoogle Scholar
  20. 21.
    Ramotar D, Popoff SC, Gralla EB et al. Cellular role of yeast Apn1 apurinic endonuclease/3′-diesterase: Repair of oxidative and alkylation DNA damage and control of spontaneous mutation. Mol Cell Biol 1991; 11:4537–4544.PubMedGoogle Scholar
  21. 22.
    Ide H, Tedzuka K, Shimzu H et al. Alpha-deoxyadenosine, a major anoxic radiolysis product of adenine in DNA, is a substrate for Escherichia coli endonuclease IV. Biochemistry 1994; 33:7842–7847.PubMedCrossRefGoogle Scholar
  22. 23.
    Yajima H, Takao M, Yasuhira S et al. A eukaryotic gene encoding an endonuclease that specifically repairs DNA damaged by ultraviolet light. EMBO J 1995; 14:2393–2399.PubMedGoogle Scholar
  23. 24.
    Klungland A, Lindahl T. Second pathway for completion of human DNA base excision-repair: Reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO j 1997; 16:3341–3348.PubMedCrossRefGoogle Scholar
  24. 25.
    Bjelland S, Seeberg E. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 2003; 531:37–80.PubMedGoogle Scholar
  25. 26.
    Dizdaroglu M, Holwitt E, Hagan MP et al. Formation of cytosine glycol and 5,6-dihydroxycytosine in deoxyribonucleic acid on treatment with osmium tetroxide. Biochem J 1986; 235:531–536.PubMedGoogle Scholar
  26. 27.
    Kasai H, Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res 1984; 12:2137–2145.PubMedCrossRefGoogle Scholar
  27. 28.
    Gros L, Ishchenko AA, Saparbaev M. Enzymology of repair of etheno-adducts. Mutat Res 2003; 531:219–229.PubMedGoogle Scholar
  28. 29.
    Jorgensen TJ, Furlong EA, Henner WD. Gamma endonuclease of Micrococcus luteus: Action on irradiated DNA. Radiat Res 1988; 114:556–566.PubMedCrossRefGoogle Scholar
  29. 30.
    Lesiak KB, Wheeler KT. Formation of alpha-deoxyadenosine in polydeoxynucleotides exposed to ionizing radiation under anoxic conditions. Radiat Res 1990; 121:328–337.PubMedCrossRefGoogle Scholar
  30. 31.
    Dizdaroglu M, Laval J, Boiteux S. Substrate specificity of the Escherichia coli endonuclease III: Excision of thymine-and cytosine-derived lesions in DNA produced by radiation-generated free radicals. Biochemistry 1993; 32:12105–12111.PubMedCrossRefGoogle Scholar
  31. 32.
    Bonicel A, Mariaggi N, Hughes E et al. In vitro gamma irradiation of DNA: Identification of radioinduced chemical modifications of the adenine moiety. Radiat Res 1980; 83:19–26.PubMedCrossRefGoogle Scholar
  32. 33.
    Akhlaq MS, Schuchman HP, von Sonntag C. The reverse of the ‘repair’ reaction of thiols: H-abstraction at carbon by thiyl radicals. Int J Radiat Biol Relat Stud Phys Chem Med 1987; 51:91–102.PubMedCrossRefGoogle Scholar
  33. 34.
    Shimizu H, Yagi R, Kimura Y et al. Replication bypass and mutagenic effect of alpha-deoxyadenosine site-specifically incorporated into single-stranded vectors. Nucleic Acids Res 1997; 25:597–603.PubMedCrossRefGoogle Scholar
  34. 35.
    Pfeifer GP. Involvement of DNA damage and repair in mutational spectra. Mutat Res 2000; 450:1–3.PubMedGoogle Scholar
  35. 36.
    Grollman AP, Moriya M. Mutagenesis by 8-oxoguanine: An enemy within. Trends Genet 1993; 9:246–249.PubMedCrossRefGoogle Scholar
  36. 37.
    Kreutzer DA, Essigmann JM. Oxidized, deaminated cytosines are a source of C→T transitions in vivo. Proc Natl Acad Sci USA 1998; 95:3578–3582.PubMedCrossRefGoogle Scholar
  37. 38.
    Wagner JR, Hu CC, Ames BN. Endogenous oxidative damage of deoxycytidine in DNA. Proc Natl Acad Sci USA 1992; 89:3380–3384.PubMedCrossRefGoogle Scholar
  38. 39.
    Ward JF. Complexity of damage produced by ionizing radiation. Cold Spring Harb Symp Quant Biol 2000; 65:377–382.PubMedCrossRefGoogle Scholar
  39. 40.
    Bennett PV, Cintron NS, Gros L et al. Are endogenous clustered DNA damages induced in human cells? Free Radic Biol Med 2004; 37:488–499.PubMedCrossRefGoogle Scholar
  40. 41.
    Harrison L, Hatahet Z, Wallace SS. In vitro repair of synthetic ionizing radiation-induced multiply damaged DNA sites. J Mol Biol 1999; 290:667–684.PubMedCrossRefGoogle Scholar
  41. 42.
    Gulston M, de Lara C, Jenner T et al. Processing of clustered DNA damage generates additional double-strand breaks in mammalian cells post-irradiation. Nucleic Acids Res 2004; 32:1602–1609.PubMedCrossRefGoogle Scholar
  42. 43.
    D’souza DI, Harrison L. Repair of clustered uracil DNA damages in Escherichia coli. Nucleic Acids Res 2003; 31:4573–4581.CrossRefGoogle Scholar
  43. 44.
    Ljungquist S. A new endonuclease from Escherichia coli acting at apurinic sites in DNA. J Biol Chem 1977; 252:2808–2814.PubMedGoogle Scholar
  44. 45.
    Levin JD, Shapiro R, Demple B. Metalloenzymes in DNA repair. Escherichia coli endonuclease IV and Saccharomyces cerevisiae. Apn1. J Biol Chem 1991; 266:22893–22898.Google Scholar
  45. 46.
    Hosfield DJ, Guan Y, Haas BJ et al. Structure of the DNA repair enzyme endonuclease IV and its DNA complex: Double-nucleotide flipping at abasic sites and three-metal-ion catalysis. Cell 1999; 98:397–408.PubMedCrossRefGoogle Scholar
  46. 47.
    Demple B, Harrison L. Repair of oxidative damage to DNA: Enzymology and biology. Annu Rev Biochem 1994; 63:915–948.PubMedCrossRefGoogle Scholar
  47. 48.
    Nunoshiba T, Ishida R, Sasaki M et al. A novel Nudix hydrolase for oxidized purine nucleoside triphosphates encoded by ORFYLR151c (PCD1 gene) in Saccharomyces cerevisiae. Nucleic Acids Res 2004; 32:5339–5348.PubMedCrossRefGoogle Scholar
  48. 49.
    Ishchenko AA, Ide H, Ramotar D et al. Alpha-anomeric deoxynucleotides, anoxic products of ionizing radiation, are substrates for the endonuclease IV-type AP endonucleases. Biochemistry 2004; 43:15210–15216.PubMedCrossRefGoogle Scholar
  49. 50.
    Ramotar D. The apurinic-apyrimidinic endonuclease IV family of DNA repair enzymes. Biochem Cell Biol 1997; 75:327–336.PubMedCrossRefGoogle Scholar
  50. 51.
    Vongsamphanh R, Fortier PK, Ramotar D. Pir1p mediates translocation of the yeast Apn1p endonuclease into the mitochondria to maintain genomic stability. Mol Cell Biol 2001; 21:1647–1655.PubMedCrossRefGoogle Scholar
  51. 52.
    Popoff SC, Spira AI, Johnson AW et al. Yeast structural gene (APN1) for the major apurinic endonuclease: Homology to Escherichia coli endonuclease IV. Proc Natl Acad Sci USA 1990; 87:4193–4197.PubMedCrossRefGoogle Scholar
  52. 53.
    Johnson AW, Demple B. Yeast DNA 3′-repair diesterase is the major cellular apurinic/apyrimidinic endonuclease: Substrate specificity and kinetics. J Biol Chem 1988; 263:18017–18022.PubMedGoogle Scholar
  53. 54.
    Johnson AW, Demple B. Yeast DNA diesterase for 3′-fragments of deoxyribose: Purification and physical properties of a repair enzyme for oxidative DNA damage. J Biol Chem 1988; 263:18009–18016.PubMedGoogle Scholar
  54. 55.
    Kunz BA, Henson ES, Roche H et al. Specificity of the mutator caused by deletion of the yeast structural gene (APN1) for the major apurinic endonuclease. Proc Natl Acad Sci USA 1994; 91:8165–8169.PubMedCrossRefGoogle Scholar
  55. 56.
    Unk I, Haracska L, Prakash S et al. 3′-phosphodiesterase and 3′→5′ exonuclease activities of yeast Apn2 protein and requirement of these activities for repair of oxidative DNA damage. Mol Cell Biol 2001; 21:1656–1661.PubMedCrossRefGoogle Scholar
  56. 57.
    Xanthoudakis S, Miao G, Wang F et al. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J 1992; 11:3323–3335.PubMedGoogle Scholar
  57. 58.
    Wilson IIIrd DM, Barsky D. The major human abasic endonuclease: Formation, consequences and repair of abasic lesions in DNA. Mutat Res. 2001; 485:283–307.PubMedGoogle Scholar
  58. 59.
    Beernink PT, Segelke BW, Hadi MZ et al. Two divalent metal ions in the active site of a new crystal form of human apurinic/apyrimidinic endonuclease, Apel: Implications for the catalytic mechanism. J Mol Biol 2001; 307:1023–1034.PubMedCrossRefGoogle Scholar
  59. 60.
    Strauss PR, Beard WA, Patterson TAeet al. Substrate binding by human apurinic/apyrimidinic endonuclease indicates a Briggs-Haldane mechanism. J Biol Chem 1997; 272:1302–1307.PubMedCrossRefGoogle Scholar
  60. 61.
    Masuda Y, Bennett RA, Demple B. Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium. J Biol Chem 1998; 273:30360–30365.PubMedCrossRefGoogle Scholar
  61. 62.
    Hadi MZ, Wilson IIIrd DM. Second human protein with homology to the Escherichia coli abasic endonuclease exonuclease III. Environ Mol Mutagen 2000; 36:312–324.PubMedCrossRefGoogle Scholar
  62. 63.
    Burkovics P, Szukacsov V, Unk I et al. Human Ape2 protein has a 3′–5′ exonuclease activity that acts preferentially on mismatched base pairs. Nucleic Acids Res 2006; 34:2508–2515.PubMedCrossRefGoogle Scholar
  63. 64.
    Ide Y, Tsuchimoto D, Tominaga Y et al. Growth retardation and dyslymphopoiesis accompanied by G2/M arrest in APEX2-null mice. Blood 2004; 104:4097–4103.PubMedCrossRefGoogle Scholar
  64. 65.
    Ischenko AA, Sanz G, Privezentzev CV et al. Characterisation of new substrate specificities of Escherichia coli and Saccharomyces cerevisiae AP endonucleases. Nucleic Acids Res 2003; 31:6344–6353.CrossRefGoogle Scholar
  65. 66.
    Gu L, Huang SM, Sander m. Single amino acid changes alter the repair specificity of Drosophila Rrp1. Isolation of mutants deficient in repair of oxidative DNA damage. J Biol Chem 1994; 269:32685–32692.PubMedGoogle Scholar
  66. 67.
    Izumi T, Ishizaki K, Ikenaga M et al. A mutant endonuclease IV of Escherichia coli loses the ability to repair lethal DNA damage induced by hydrogen peroxide but not that induced by methyl methanesulfonate. J Bacteriol 1992; 174:7711–7716.PubMedGoogle Scholar
  67. 68.
    Yang X, Tellier P, Masson JY et al. Characterization of amino acid substitutions that severely alter the DNA repair functions of Escherichia coli endonuclease IV. Biochemistry 1999; 38:3615–3623.PubMedCrossRefGoogle Scholar
  68. 69.
    Fung H, Demple B. A vital role for Ape1/Ref1 protein in repairing spontaneous DNA damage in human cells. Mol Cell 2005; 17:463–470.PubMedCrossRefGoogle Scholar
  69. 70.
    Izumi T, Brown DB, Naidu CV et al. Two essential but distinct functions of the mammalian abasic endonuclease. Proc Natl Acad Sci USA 2005; 102:5739–5743.PubMedCrossRefGoogle Scholar
  70. 71.
    Meira LB, Devaraj S, Kisby GE et al. Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress. Cancer Res 2001; 61:5552–5557.PubMedGoogle Scholar
  71. 72.
    Maksimenko A, Ishchenko AA, Sanz G et al. A molecular beacon assay for measuring base excision repair activities. Biochem Biophys Res Commun 2004; 319:240–246.PubMedCrossRefGoogle Scholar
  72. 73.
    Ikeda S, Biswas T, Roy R et al. Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue. J Biol Chem 1998; 273:21585–21593.PubMedCrossRefGoogle Scholar
  73. 74.
    Mol CD, Izumi T, Mitra S et al. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected]. Nature 2000; 403:451–456.PubMedCrossRefGoogle Scholar
  74. 75.
    Hang B, Chenna A, Fraenkel-Conrat H et al. An unusual mechanism for the major human apurinic/apyrimidinic (AP) endonuclease involving 5′ cleavage of DNA containing a benzene-derived exocyclic adduct in the absence of an AP site. Proc Natl Acad Sci USA 1996; 93:13737–13741.PubMedCrossRefGoogle Scholar
  75. 76.
    Chou KM, Cheng YC. The exonuclease activity of human apurinic/apyrimidinic endonuclease (APE1). Biochemical properties and inhibition by the natural dinucleotide Gp4G. J Biol Chem 2003; 278:18289–18296.PubMedCrossRefGoogle Scholar
  76. 77.
    Chou KM, Cheng YC. An exonucleolytic activity of human apurinic/apyrimidinic endonuclease on 3′ mispaired DNA. Nature 2002; 415:655–659.PubMedCrossRefGoogle Scholar
  77. 78.
    Ishchenko AA, Yang X, Ramotar D et al. The 3′→5′ Exonuclease of Apn1 provides an alternative pathway to repair 7,8-Dihydro-8-Oxodeoxyguanosine in Saccharomyces cerevisiae. Mol Cell Biol 2005; 25:6380–6390.PubMedCrossRefGoogle Scholar
  78. 79.
    Kamath-Loeb AS, Hizi A, Kasai H et al. Incorporation of the guanosine triphosphate analogs 8-oxo-dGTP and 8-NH2-dGTP by reverse transcriptases and mammalian DNA polymerases. J Biol Chem 1997; 272:5892–5898.PubMedCrossRefGoogle Scholar
  79. 80.
    Miller H, Prasad R, Wilson SH et al. 8-oxodGTP incorporation by DNA polymerase beta is modified by active-site residue Asn279. Biochemistry 2000; 39:1029–1033.PubMedCrossRefGoogle Scholar
  80. 81.
    Burkart W, Jung T, Frasch G. Damage pattern as a function of radiation quality and other factors. CR Acad Sci III 1999; 322:89–101.Google Scholar
  81. 82.
    Parsons JL, Dianova II, Dianov GL. APE1-dependent repair of DNA single-strand breaks containing 3′-end 8-oxoguanine. Nucleic Acids Res 2005; 33:2204–2209.PubMedCrossRefGoogle Scholar
  82. 83.
    Klungland A, Rosewell I, Hollenbach S et al. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc Natl Acad Sci USA 1999; 96:13300–13305.PubMedCrossRefGoogle Scholar
  83. 84.
    Minowa O, Arai T, Hirano M et al. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc Natl Acad Sci USA 2000; 97:4156–4161.PubMedCrossRefGoogle Scholar
  84. 85.
    Kerins SM, Collins R, McCarthy TV. Characterization of an endonuclease IV 3′–5′ exonuclease activity. J Biol Chem 2003; 278:3048–3054.PubMedCrossRefGoogle Scholar
  85. 86.
    Sung JS, Mosbaugh DW. Escherichia coli uracil-and ethenocytosine-initiated base excision DNA repair: Rate-limiting step and patch size distribution. Biochemistry 2003; 42:4613–4625.PubMedCrossRefGoogle Scholar
  86. 87.
    Levin JD, Demple B. In vitro detection of endonuclease IV-specific DNA damage formed by bleomycin in vivo. Nucleic Acids Res 1996; 24:885–889.PubMedCrossRefGoogle Scholar
  87. 88.
    Povirk LF. DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: Bleomycin, neocarzinostatin and other enediynes. Mutat Res 1996; 355:71–89.PubMedGoogle Scholar
  88. 89.
    Parsons JL, Zharkov DO, Dianov GL. NEIL1 excises 3′ end proximal oxidative DNA lesions resistant to cleavage by NTH1 and OGGI. Nucleic Acids Res 2005; 33:4849–4856.PubMedCrossRefGoogle Scholar
  89. 90.
    Harrison L, Skorvaga M, Cunningham RP et al. Transfection of the Escherichia coli nth gene into radiosensitive Chinese hamster cells: Effects on sensitivity to radiation, hydrogen peroxide, and bleomycin sulfate. Radiat Res 1992; 132:30–39.PubMedCrossRefGoogle Scholar
  90. 91.
    Friedberg EC. Suffering in silence: The tolerance of DNA damage. Nat Rev Mol Cell Biol 2005; 6:943–953.PubMedCrossRefGoogle Scholar
  91. 92.
    Sabbioneda S, Minesinger BK, Giannattasio M et al. The 9-1-1 checkpoint clamp physically interacts with polzeta and is partially required for spontaneous polzeta-dependent mutagenesis in Saccharomyces cerevisiae. J Biol Chem 2005; 280:38657–38665.PubMedCrossRefGoogle Scholar
  92. 93.
    Haracska L, Unk I, Prakash L et al. Ubiquitylation of yeast proliferating cell nuclear antigen and its implications for translesion DNA synthesis. Proc Natl Acad Sci USA 2006; 103:6477–6482.PubMedCrossRefGoogle Scholar
  93. 94.
    Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K et al. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39–85.PubMedCrossRefGoogle Scholar
  94. 95.
    Evans AR, Limp-Foster M, Kelley MR. Going APE over ref-1. Mutat Res 2000; 461:83–108.PubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2007

Authors and Affiliations

  • Sophie Couvé-Privat
    • 1
  • Alexander A. Ishchenko
    • 1
  • Jacques Laval
    • 1
  • Murat Saparbaev
    • 1
  1. 1.Groupe “Réparation de ľADN”, UMR 8126 CNRSUniv Paris-Sud, Institut Gustave RoussyVillejuif CedexFrance

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