Targeting base excision repair to improve cancer therapies

Molecular Aspects of Medicine - Tập 28 - Trang 345-374 - 2007
Ricky A. Sharma1, Grigory L. Dianov2
1Radiation Oncology & Biology, University of Oxford, Churchill Hospital, Oxford OX3 7LJ, UK
2Radiation Oncology & Biology, University of Oxford, MRC Harwell, Didcot, Oxfordshire OX11 0RD, UK

Tài liệu tham khảo

Aaltonen, 2007, Explaining the familial colorectal cancer risk associated with mismatch repair (MMR)-deficient and MMR-stable tumors, Clin. Cancer Res., 13, 356, 10.1158/1078-0432.CCR-06-1256 Ahel, 2006, The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates, Nature, 443, 713, 10.1038/nature05164 Albertella, 2005, A role for polymerase eta in the cellular tolerance to cisplatin-induced damage, Cancer Res., 65, 9799, 10.1158/0008-5472.CAN-05-1095 Albertella, 2005, The overexpression of specialized DNA polymerases in cancer, DNA Repair (Amst.), 4, 583, 10.1016/j.dnarep.2005.01.005 Allinson, 2003, Poly(ADP-ribose)polymerase in base excision repair: always engaged, but not essential for DNA damage processing, Acta Biochim. Pol., 50, 169, 10.18388/abp.2003_3724 Ame, 2004, The PARP superfamily, Bioessays, 26, 882, 10.1002/bies.20085 Aoufouchi, 1999, Inhibition of apoptosis of a PARP(−/−) cell line transfected with PARP DNA-binding domain mutants, J. Mol. Biol., 290, 943, 10.1006/jmbi.1999.2930 Aspinwall, 1997, Cloning and characterization of a functional human homolog of Escherichia coli endonuclease III, Proc. Natl. Acad. Sci. USA, 94, 109, 10.1073/pnas.94.1.109 Avkin, 2006, p53 and p21 regulate error-prone DNA repair to yield a lower mutation load, Mol. Cell, 22, 407, 10.1016/j.molcel.2006.03.022 Barnes, 1992, Mutations in the DNA ligase I gene of an individual with immunodeficiencies and cellular hypersensitivity, Cell, 69, 495, 10.1016/0092-8674(92)90450-Q Bassett, 2003, Efficiency of extension of mismatched primer termini across from cisplatin and oxaliplatin adducts by human DNA polymerases beta and eta in vitro, Biochemistry, 42, 14197, 10.1021/bi035359p Bassett, 2004, The role of DNA polymerase eta in translesion synthesis past platinum–DNA adducts in human fibroblasts, Cancer Res., 64, 6469, 10.1158/0008-5472.CAN-04-1328 Beneke, 2001, Inhibition of poly(ADP-ribose)polymerase activity accelerates T-cell lymphomagenesis in p53 deficient mice, Oncogene, 20, 8136, 10.1038/sj.onc.1205056 Bennett, 2001, Fidelity of uracil-initiated base excision DNA repair in DNA polymerase beta-proficient and -deficient mouse embryonic fibroblast cell extracts, J. Biol. Chem., 276, 42588, 10.1074/jbc.M106212200 Bergoglio, 2001, Enhanced expression and activity of DNA polymerase beta in human ovarian tumor cells: impact on sensitivity towards antitumor agents, Oncogene, 20, 6181, 10.1038/sj.onc.1204743 Boorstein, 2001, Definitive identification of mammalian 5-hydroxymethyluracil DNA N-glycosylase activity as SMUG1, J. Biol. Chem., 276, 41991, 10.1074/jbc.M106953200 Bowman, 2001, Differential effects of the poly(ADP-ribose)polymerase (PARP) inhibitor NU1025 on topoisomerase I and II inhibitor cytotoxicity in L1210 cells in vitro, Br. J. Cancer, 84, 106, 10.1054/bjoc.2000.1555 Brenner, 2002, Hint, Fhit, and GalT: function, structure, evolution, and mechanism of three branches of the histidine triad superfamily of nucleotide hydrolases and transferases, Biochemistry, 41, 9003, 10.1021/bi025942q Brock, 2004, Radiosensitization of human and rodent cell lines by INO-1001, a novel inhibitor of poly(ADP-ribose)polymerase, Cancer Lett., 205, 155, 10.1016/j.canlet.2003.10.029 Bryant, 2005, Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose)polymerase, Nature, 434, 913, 10.1038/nature03443 Calabrese, 2004, Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose)polymerase-1 inhibitor AG14361, J. Natl. Cancer Inst., 96, 56, 10.1093/jnci/djh005 Caldecott, 2003, DNA single-strand break repair and spinocerebellar ataxia, Cell, 112, 7, 10.1016/S0092-8674(02)01247-3 Caldecott, 1994, An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III, Mol Cell Biol, 14, 68, 10.1128/MCB.14.1.68 Caldecott, 1995, Characterization of the XRCC1–DNA ligase III complex in vitro and its absence from mutant hamster cells, Nucleic Acid Res., 23, 4836, 10.1093/nar/23.23.4836 Caldecott, 1996, XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly(ADP-ribose)polymerase, and DNA ligase III is a novel molecular ‘nick-sensor’ in vitro, Nucleic Acid Res., 24, 4387, 10.1093/nar/24.22.4387 Canitrot, 1998, Overexpression of DNA polymerase beta in cell results in a mutator phenotype and a decreased sensitivity to anticancer drugs, Proc. Natl. Acad. Sci. USA, 95, 12586, 10.1073/pnas.95.21.12586 Canitrot, 1999, Overexpression of DNA polymerase beta: a genomic instability enhancer process, FASEB J., 13, 1107, 10.1096/fasebj.13.9.1107 Cappelli, 1997, Involvement of XRCC1 and DNA ligase III gene products in DNA base excision repair, J. Biol. Chem., 272, 23970, 10.1074/jbc.272.38.23970 Chakravarti, 1991, Cloning and expression in Escherichia coli of a human cDNA encoding the DNA repair protein N-methylpurine-DNA glycosylase, J. Biol. Chem., 266, 15710, 10.1016/S0021-9258(18)98467-X Chaney, 2005, Recognition and processing of cisplatin– and oxaliplatin–DNA adducts, Crit. Rev. Oncol. Hematol., 53, 3, 10.1016/j.critrevonc.2004.08.008 Chen, 1991, Two distinct human diesterases that hydrolyze 3′-blocking deoxyribose fragments from oxidised DNA, Nucleic Acid Res., 19, 5907, 10.1093/nar/19.21.5907 Clements, 2004, The ataxia-oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4, DNA Repair (Amst.), 3, 1493, 10.1016/j.dnarep.2004.06.017 Conde, 2001, Loss of poly(ADP-ribose)polymerase-1 causes increased tumour latency in p53-deficient mice, EMBO J., 20, 3535, 10.1093/emboj/20.13.3535 Dalal, 2005, Prostate-cancer-associated I260M variant of DNA polymerase beta is a sequence-specific mutator, Biochemistry, 44, 15664, 10.1021/bi051179z Date, 2004, The FHA domain of aprataxin interacts with the C-terminal region of XRCC1, Biochem. Biophys. Res. Commun., 325, 1279, 10.1016/j.bbrc.2004.10.162 Delaney, 2000, Potentiation of temozolomide and topotecan growth inhibition and cytotoxicity by novel poly(adenosine diphosphoribose) polymerase inhibitors in a panel of human tumor cell lines, Clin. Cancer Res., 6, 2860 DeMott, 1998, Replication protein a stimulates long patch DNA base excision repair, J. Biol. Chem., 273, 27492, 10.1074/jbc.273.42.27492 Demple, 1991, Cloning and expression of APE, the cDNA encoding the major human apurinic endonuclease: definition of a family of DNA epair enzymes, Proc. Natl. Acad. Sci. USA, 88, 11450, 10.1073/pnas.88.24.11450 de Souza-Pinto, 2001, Repair of 8-oxodeoxyguanosine lesions in mitochondrial DNA depends on the oxoguanine DNA glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial DNA of OGG1-defective mice, Cancer Res., 61, 5378 Dianova, 2004, XRCC1–DNA polymerase beta interaction is required for efficient base excision repair, Nucleic Acid Res., 32, 2550, 10.1093/nar/gkh567 Dianov, 1992, Generation of single-nucleotide repair patches following excision of uracil residues from DNA, Mol. Cell. Biol., 12, 1605, 10.1128/MCB.12.4.1605 Dianov, 1999, Replication protein a stimulates proliferating cell nuclear antigen-dependent repair of abasic sites in DNA by human cell extracts, Biochemistry, 38, 11021, 10.1021/bi9908890 Dianov, 2001, Base excision repair in nuclear and mitochondrial DNA, Prog. Nucleic Acid Res. Mol. Biol., 68, 285, 10.1016/S0079-6603(01)68107-8 Dou, 2003, Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2, J. Biol. Chem., 278, 49679, 10.1074/jbc.M308658200 Eastman, 1987, The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes, Pharmacol. Ther., 34, 155, 10.1016/0163-7258(87)90009-X Eberhart, 2003, Medulloblastoma in mice lacking p53 and PARP: all roads lead to Gli, Am. J. Pathol., 162, 7, 10.1016/S0002-9440(10)63792-3 Elder, 2002, Repair of dihydrouracil supported by base excision repair in mNTH1 knock-out cell extracts, J. Biol. Chem., 277, 50487, 10.1074/jbc.M208153200 Engelward, 1997, Base excision repair deficient mice lacking the Aag alkyladenine DNA glycosylase, Proc. Natl. Acad. Sci. USA, 94, 13087, 10.1073/pnas.94.24.13087 Evans, 2000, Going APE over ref-1, Mutat. Res., 461, 83, 10.1016/S0921-8777(00)00046-X Fan, 2004, XRCC1 co-localizes and physically interacts with PCNA, Nucleic Acid Res., 32, 2193, 10.1093/nar/gkh556 Farmer, 2005, Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy, Nature, 434, 917, 10.1038/nature03445 Farrington, 2005, Germline susceptibility to colorectal cancer due to base-excision repair gene defects, Am. J. Hum. Genet., 77, 112, 10.1086/431213 Fishel, 2007, Manipulation of base excision repair to sensitize ovarian cancer cells to alkylating agent temozolomide, Clin. Cancer Res., 13, 260, 10.1158/1078-0432.CCR-06-1920 Fortini, 2007, Base damage and single-strand break repair: mechanisms and functional significance of short- and long-patch repair subpathways, DNA Repair (Amst.), 6, 398, 10.1016/j.dnarep.2006.10.008 Friday, 2005, K-ras as a target for cancer therapy, Biochim. Biophys. Acta, 1756, 127 Frosina, 1996, Two pathways for base excision repair in mammalian cells, J. Biol. Chem., 271, 9573, 10.1074/jbc.271.16.9573 Fung, 2005, A vital role for ape1/ref1 protein in repairing spontaneous DNA damage in human cells, Mol. Cell, 17, 463, 10.1016/j.molcel.2004.12.029 Glassner, 1998, Generation of a strong mutator phenotype in yeast by imbalanced base excision repair, Proc. Natl. Acad. Sci. USA, 95, 9997, 10.1073/pnas.95.17.9997 Gryk, 2002, Mapping of the interaction interface of DNA polymerase beta with XRCC1, Structure (Camb.), 10, 1709, 10.1016/S0969-2126(02)00908-5 Gu, 1994, Deletion of a DNA-polymerase-beta gene segment in T-cells using cell-type-specific gene targeting, Science, 265, 103, 10.1126/science.8016642 Gueven, 2004, Aprataxin, a novel protein that protects against genotoxic stress, Hum. Mol. Genet., 13, 1081, 10.1093/hmg/ddh122 Hadi, 2002, Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III, J. Mol. Biol., 316, 853, 10.1006/jmbi.2001.5382 Hang, 1997, Targeted deletion of alkylpurine-DNA-N-glycosylase in mice eliminates repair of 1,N-6-ethenoadenine and hypoxanthine but not of 3,N-4-ethenocytosine or 8-oxoguanine, Proc. Natl. Acad. Sci. USA, 94, 12869, 10.1073/pnas.94.24.12869 Harrison, 2002, Replicatuion failure, genome instability, and increased cancer susceptibility in mice with a point mutation in the DNA ligase I gene, Cancer Res., 62, 4065 Haushalter, 1999, Identification of a new uracil–DNA glycosylase family by expression cloning using synthetic inhibitors, Curr. Biol., 9, 174, 10.1016/S0960-9822(99)80087-6 Havener, 2003, Translesion synthesis past platinum DNA adducts by human DNA polymerase mu, Biochemistry, 42, 1777, 10.1021/bi0270079 Hecht, 1999, Tobacco smoke carcinogens and lung cancer, J. Natl. Cancer Inst., 91, 1194, 10.1093/jnci/91.14.1194 Hendrich, 1999, The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites, Nature, 401, 301, 10.1038/45843 Herceg, 2001, Functions of poly(ADP-ribose)polymerase (PARP) in DNA repair, genomic integrity and cell death, Mutat. Res., 477, 97, 10.1016/S0027-5107(01)00111-7 Hirose, 1989, Difference in the expression level of DNA polymerase beta among mouse tissues: high expression in the pachytene spermatocyte, Exp. Cell Res., 181, 169, 10.1016/0014-4827(89)90191-2 Hong, 2004, Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling, Trend Pharmacol. Sci., 25, 259, 10.1016/j.tips.2004.03.005 Hung, 2005, Genetic polymorphisms in the base excision repair pathway and cancer risk: a HuGE review, Am. J. Epidemiol., 162, 925, 10.1093/aje/kwi318 Iizuka, 2006, Involvement of c-myc-regulated genes in hepatocellular carcinoma related to genotype-C hepatitis B virus, J. Cancer Res. Clin. Oncol., 132, 473, 10.1007/s00432-006-0094-8 Ikeda, 1998, 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., 273, 21585, 10.1074/jbc.273.34.21585 Izumi, 2005, Two essential but distinct functions of the mammalian abasic endonuclease, Proc. Natl. Acad. Sci. USA, 102, 5739, 10.1073/pnas.0500986102 Jagtap, 2005, Poly(ADP-ribose)polymerase and the therapeutic effects of its inhibitors, Nat. Rev. Drug Discov., 4, 421, 10.1038/nrd1718 Jaruga, 2004, Mouse NEIL1 protein is specific for excision of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 4,6-diamino-5-formamidopyrimidine from oxidatively damaged DNA, Biochemistry, 43, 15909, 10.1021/bi048162l Jilani, 1999, Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3′-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage, J. Biol. Chem., 274, 24176, 10.1074/jbc.274.34.24176 Jones, 2002, Biallelic germline mutations in MYH predispose to multiple colorectal adenoma and somatic G:C→T:A mutations, Hum. Mol. Genet., 11, 2961, 10.1093/hmg/11.23.2961 Kakolyris, 1998, Expression and subcellular localisation of human AP endonuclease 1 (HAP1/Ref-1) protein: a basis for its role in human disease, Histopathology, 33, 561, 10.1046/j.1365-2559.1998.00541.x Karimi-Busheri, 1999, Molecular characterization of a human DNA kinase, J. Biol. Chem., 274, 24187, 10.1074/jbc.274.34.24187 Kijas, 2006, Aprataxin forms a discrete branch in the HIT (histidine triad) superfamily of proteins with both DNA/RNA binding and nucleotide hydrolase activities, J. Biol. Chem., 281, 13939, 10.1074/jbc.M507946200 Klungland, 1997, Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1), EMBO J., 16, 3341, 10.1093/emboj/16.11.3341 Klungland, 1997, Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1), EMBO J., 16, 3341, 10.1093/emboj/16.11.3341 Klungland, 1999, Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage, Proc. Natl. Acad. Sci. USA, 96, 13300, 10.1073/pnas.96.23.13300 Krokan, 2001, Properties and functions of human uracil-DNA glycosylase from the UNG gene, Prog. Nucleic Acid Res. Mol. Biol., 68, 365, 10.1016/S0079-6603(01)68112-1 Kubota, 2003, Independent roles of XRCC1’s two BRCT motifs in recovery from methylation damage, DNA Repair (Amst.), 2, 407, 10.1016/S1568-7864(02)00242-2 Kubota, 1996, Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase β and the XRCC1 protein, EMBO J., 15, 6662, 10.1002/j.1460-2075.1996.tb01056.x Kumar, 1990, Studies of the domain structure of mammalian DNA polymerase beta. Identification of a discrete template binding domain, J. Biol. Chem., 265, 2124, 10.1016/S0021-9258(19)39949-1 Levin, 2000, Interaction between PCNA and DNA ligase I is critical for joining of Okazaki fragments and long-patch base-excision repair, Curr. Biol., 10, 919, 10.1016/S0960-9822(00)00619-9 Lindahl, 1993, Instability and decay of the primary structure of DNA, Nature, 362, 709, 10.1038/362709a0 Lindahl, 1999, Quality control by DNA repair, Science, 286, 1897, 10.1126/science.286.5446.1897 Lis, 2006, Promoter cleavage: a topoIIbeta and PARP-1 collaboration, Cell, 125, 1225, 10.1016/j.cell.2006.06.016 Liu, 2004, Therapeutic impact of methoxyamine: blocking repair of abasic sites in the base excision repair pathway, Curr. Opin. Invest. Drug, 5, 623 Liu, 1999, Pharmacologic disruption of base excision repair sensitizes mismatch repair-deficient and -proficient colon cancer cells to methylating agents, Clin. Cancer Res., 5, 2908 Liu, 2002, Base excision repair as a therapeutic target in colon cancer, Clin. Cancer Res., 8, 2985 Ljungquist, 1994, Altered DNA ligase III activity in the CHO EM9 mutant, Mutat. Res., 314, 177, 10.1016/0921-8777(94)90081-7 Luo, 2004, Inhibition of the human apurinic/apyrimidinic endonuclease (APE1) repair activity and sensitization of breast cancer cells to DNA alkylating agents with lucanthone, Anticancer Res., 24, 2127 Mackey, 1997, An alternative splicing event which occurs in mouse pachytene spermatocytes generates a form of DNA ligase III with distinct biochemical properties that may function in meiotic recombination, Mol. Cell. Biol., 17, 989, 10.1128/MCB.17.2.989 Madhusudan, 2005, The emerging role of DNA repair proteins as predictive, prognostic and therapeutic targets in cancer, Cancer Treat. Rev., 31, 603, 10.1016/j.ctrv.2005.09.006 Madhusudan, 2005, Isolation of a small molecule inhibitor of DNA base excision repair, Nucleic Acid Res., 33, 4711, 10.1093/nar/gki781 Marintchev, 1999, Solution structure of the single-strand break repair protein XRCC1 N- terminal domain, Nat. Struct. Biol., 6, 884, 10.1038/12347 Marintchev, 2000, Domain specific interaction in the XRCC1–DNA polymerase beta complex, Nucleic Acid Res., 28, 2049, 10.1093/nar/28.10.2049 Masson, 1998, XRCC1 is specifically associated with poly(ADP-ribose)polymerase and negatively regulates its activity following DNA damage, Mol. Cell. Biol., 18, 3563, 10.1128/MCB.18.6.3563 Matsumoto, 1995, Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair, Science, 269, 699, 10.1126/science.7624801 Matsumoto, 1995, Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair, Science, 269, 699, 10.1126/science.7624801 Matsuzaki, 1996, DNA polymerase beta gene mutations in human bladder cancer, Mol. Carcinogen., 15, 38, 10.1002/(SICI)1098-2744(199601)15:1<38::AID-MC6>3.0.CO;2-O McCullough, 1999, Initiation of base excision repair: glycosylase mechanism and structure, Annu. Rev. Biochem., 68, 255, 10.1146/annurev.biochem.68.1.255 Menegazzi, 1999, Correlation of poly(ADP-ribose)polymerase and p53 expression levels in high-grade lymphomas, Mol. Carcinogen., 25, 256, 10.1002/(SICI)1098-2744(199908)25:4<256::AID-MC4>3.0.CO;2-W Ménessier-de Murcia, 1997, Requirement of poly(ADP-ribose)polymerase in recovery from DNA damage in mice and in cells, Proc. Natl. Acad. Sci. USA, 94, 7303, 10.1073/pnas.94.14.7303 Menissier-de Murcia, 1997, Requirement of poly(ADP-ribose)polymerase in recovery from DNA damage in mice and in cells, Proc Natl Acad Sci USA, 94, 7303, 10.1073/pnas.94.14.7303 Millar, 2002, Enhanced CpG mutability and tumorigenesis in MBD4-deficient mice, Science, 297, 403, 10.1126/science.1073354 Minowa, 2000, MMH/OGG1 gene inactivation results in accumulation of 8-hydroxyguanine in mice, Proc. Natl. Acad. Sci. USA, 97, 4156, 10.1073/pnas.050404497 Molinete, 1993, Overproduction of the poly(adp-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA-repair synthesis in mammalian-cells, EMBO J., 12, 2109, 10.1002/j.1460-2075.1993.tb05859.x Moore, 2000, Mutation of a BRCT domain selectively disrupts DNA single-strand break repair in noncycling Chinese hamster ovary cells, Proc. Natl. Acad. Sci. USA, 97, 13649, 10.1073/pnas.250477597 Moreira, 2001, The gene mutated in ataxia-ocular apraxia 1 encodes the new HIT/Zn-finger protein aprataxin, Nat. Genet., 29, 189, 10.1038/ng1001-189 Moriya, 1993, Mutations in the MutY gene of Escherichia coli enhance the frequency of targeted G:C→T:A transversions induced by a single 8-oxoguanine residue in single-stranded DNA, Mol. Gen. Genet., 239, 72, 10.1007/BF00281603 Munoz-Gamez, 2005, PARP inhibition sensitizes p53-deficient breast cancer cells to doxorubicin-induced apoptosis, Biochem. J., 386, 119, 10.1042/BJ20040776 Nash, 1997, XRCC1 protein interacts with one of two distinct forms of DNA ligase III, Biochemistry, 36, 5207, 10.1021/bi962281m Neddermann, 1996, Cloning and expression of human G/T mismatch-specific thymine–DNA glycosylase, J. Biol. Chem., 271, 12767, 10.1074/jbc.271.22.12767 Nielsen, 2005, Multiplicity in polyp count and extracolonic manifestations in 40 Dutch patients with MYH associated polyposis coli (MAP), J. Med. Genet., 42, e54, 10.1136/jmg.2005.033217 Nilsen, 2000, Uracil–DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication, Mol. Cell, 5, 1059, 10.1016/S1097-2765(00)80271-3 Noel, 2006, Radiosensitization by the poly(ADP-ribose)polymerase inhibitor 4-amino-1,8-naphthalimide is specific of the S phase of the cell cycle and involves arrest of DNA synthesis, Mol. Cancer Ther., 5, 564, 10.1158/1535-7163.MCT-05-0418 Nosho, 2006, Overexpression of poly(ADP-ribose)polymerase-1 (PARP-1) in the early stage of colorectal carcinogenesis, Eur. J. Cancer, 42, 2374, 10.1016/j.ejca.2006.01.061 Ocampo, 2002, Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity, Mol. Cell. Biol., 22, 6111, 10.1128/MCB.22.17.6111-6121.2002 O’Connor, 1991, Human cDNA expressing a functional DNA glycosylase excising 3-methyladenine and 7-methylguanine, Biochem. Biophys. Res. Commun., 176, 1170, 10.1016/0006-291X(91)90408-Y Olsen, 1989, Molecular cloning of human uracil-DNA glycosylase, a highly conserved DNA repair enzyme, EMBO J., 8, 3121, 10.1002/j.1460-2075.1989.tb08464.x Park, 2005, Poly(ADP-ribose)polymerase-1 could facilitate the religation of topoisomerase I-linked DNA inhibited by camptothecin, Cancer Res., 65, 3894, 10.1158/0008-5472.CAN-04-4014 Parsons, 2004, APE1 is the major 3′-phosphoglycolate activity in human cell extracts, Nucleic Acid Res., 32, 3531, 10.1093/nar/gkh676 Parsons, 2005, Poly(ADP-ribose)polymerase-1 protects excessive DNA strand breaks from deterioration during repair in human cell extracts, FEBS J., 272, 2012, 10.1111/j.1742-4658.2005.04628.x Parsons, 2005, APE1-dependent repair of DNA single-strand breaks containing 3′-end 8-oxoguanine, Nucleic Acid Res., 33, 2204, 10.1093/nar/gki518 Pascucci, 1999, Long patch base excision repair with purified proteins, J. Biol. Chem., 274, 33696, 10.1074/jbc.274.47.33696 Perkins, 2001, Novel inhibitors of poly(ADP-ribose)polymerase/PARP1 and PARP2 identified using a cell-based screen in yeast, Cancer Res., 61, 4175 Peterlongo, 2006, Increased frequency of disease-causing MYH mutations in colon cancer families, Carcinogenesis, 27, 2243, 10.1093/carcin/bgl093 Petronzelli, 2000, Biphasic kinetics of the human DNA repair protein MED1 (MBD4), a mismatch-specific DNA N-glycosylase, J. Biol. Chem., 275, 32422, 10.1074/jbc.M004535200 Podlutsky, 2001, Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA, EMBO J., 20, 1477, 10.1093/emboj/20.6.1477 Podlutsky, 2001, DNA synthesis and dRPase activities of polymerase beta are both essential for single-nucleotide patch base excision repair in mammalian cell extracts, Biochemistry, 40, 809, 10.1021/bi002064s Poltoratsky, 2005, REV1 mediated mutagenesis in base excision repair deficient mouse fibroblast, DNA Repair (Amst.), 4, 1182, 10.1016/j.dnarep.2005.05.002 Prigent, 1994, Aberrant DNA repair and DNA replication due to an inherited enzymatic defect in human DNA ligase I, Mol. Cell. Biol., 14, 310, 10.1128/MCB.14.1.310 Puebla-Osorio, 2006, Early embryonic lethality due to targeted inactivation of DNA ligase III, Mol. Cell. Biol., 26, 3935, 10.1128/MCB.26.10.3935-3941.2006 Radicella, 1997, Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae, Proc. Natl. Acad. Sci. USA, 94, 8010, 10.1073/pnas.94.15.8010 Rasouli-Nia, 2004, Stable down-regulation of human polynucleotide kinase enhances spontaneous mutation frequency and sensitizes cells to genotoxic agents, Proc. Natl. Acad. Sci. USA, 101, 6905, 10.1073/pnas.0400099101 Rivkees, 1994, Expression of a multifunctional DNA-repair enzyme gene, apurinic/apyrimidinic endonuclease (Ape–Ref-1) in the suprachiasmatic, supraoptic and paraventricular nuclei, Brain Res., 666, 137, 10.1016/0006-8993(94)90296-8 Robson, 1991, Isolation of cDNA clones encoding a human apurinic/apyrimidinic endonuclease that corrects DNA repair and mutagenesis defects in E. coli xth (exonuclease III) mutants, Nucleic Acid Res., 19, 5519, 10.1093/nar/19.20.5519 Roldan-Arjona, 1997, Molecular cloning and functional expression of a human cDNA encoding the antimutator enzyme 8-hydroxyguanine–DNA glycosylase, Proc. Natl. Acad. Sci. USA, 94, 8016, 10.1073/pnas.94.15.8016 Rosenquist, 1997, Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase, Proc. Natl. Acad. Sci. USA, 94, 7429, 10.1073/pnas.94.14.7429 Sakumi, 2003, OGG1 knockout-associated lung tumorigenesis and its suppression by Mth1 gene disruption, Cancer Res., 63, 902 Samson, 1991, Cloning and characterization of a 3-methyladenine DNA glycosylase CDNA from human-cells whose gene maps to chromosome-16, Proc. Natl. Acad. Sci. USA, 88, 9127, 10.1073/pnas.88.20.9127 Sanderson, 1998, Fidelity and mutational specificity of uracil-initiated base excision DNA repair synthesis in human glioblastoma cell extracts, J. Biol. Chem., 273, 24822, 10.1074/jbc.273.38.24822 Satoh, 1992, Role of poly(ADP-ribose) formation in DNA repair, Nature, 356, 356, 10.1038/356356a0 Satoh, 1993, NAD(+)-dependent repair of damaged DNA by human cell extracts, J. Biol. Chem., 268, 5480, 10.1016/S0021-9258(18)53346-9 Sawyer, 1999, Repair of DNA damage in mitochondria, Mutat. Res.-DNA Repair, 434, 161, 10.1016/S0921-8777(99)00027-0 Sharma, 2007, Phase I trial of radioembolisation of liver metastases from colorectal cancer using yttrium-90 microspheres with concomitant systemic 5-fluorouracil/leucovorin (FOLFOX) chemotherapy, J. Clin. Oncol., 25, 1099, 10.1200/JCO.2006.08.7916 Shibata, 2005, Parp-1 deficiency causes an increase of deletion mutations and insertions/rearrangements in vivo after treatment with an alkylating agent, Oncogene, 24, 1328, 10.1038/sj.onc.1208289 Sieber, 2004, MYH deficiency enhances intestinal tumorigenesis in multiple intestinal neoplasia (ApcMin/+) mice, Cancer Res., 64, 8876, 10.1158/0008-5472.CAN-04-2958 Sleeth, 2004, Exchangeability of mammalian DNA ligases between base excision repair pathways, Biochemistry, 43, 12924, 10.1021/bi0492612 Slupska, 1996, Cloning and sequencing a human homolog (hMYH) of the Escherichia coli MutY gene whose function is required for the repair of oxidative DNA damage, J. Bacteriol., 178, 3885, 10.1128/jb.178.13.3885-3892.1996 Slupska, 1999, Functional expression of hMYH, a human homolog of the Escherichia coli MutY protein, J. Bacteriol., 181, 6210, 10.1128/JB.181.19.6210-6213.1999 Smith, 2001, The world according to PARP, Trend Biochem. Sci., 26, 174, 10.1016/S0968-0004(00)01780-1 Sobol, 1996, Requirement of mammalian DNA polymerase-β in base-excision repair, Nature, 379, 183, 10.1038/379183a0 Srivastava, 1999, DNA polymerase beta expression differences in selected human tumors and cell lines, Carcinogenesis, 20, 1049, 10.1093/carcin/20.6.1049 Staibano, 2005, Poly(adenosine diphosphate-ribose) polymerase 1 expression in malignant melanomas from photoexposed areas of the head and neck region, Hum. Pathol., 36, 724, 10.1016/j.humpath.2005.04.017 Sung, 2006, Roles of base excision repair subpathways in correcting oxidized abasic sites in DNA, FEBS J., 273, 1620, 10.1111/j.1742-4658.2006.05192.x Sweasy, 2005, Expression of DNA polymerase {beta} cancer-associated variants in mouse cells results in cellular transformation, Proc. Natl. Acad. Sci. USA, 102, 14350, 10.1073/pnas.0505166102 Szabo, 1998, Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion, Trend Pharmacol. Sci., 19, 287, 10.1016/S0165-6147(98)01193-6 Takao, 2002, Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse Nth1 gene encoding an endonuclease III homolog for repair of thymine glycols, EMBO J., 21, 3486, 10.1093/emboj/cdf350 Tan, 2005, Frequent mutation related with overexpression of DNA polymerase beta in primary tumors and precancerous lesions of human stomach, Cancer Lett., 220, 101, 10.1016/j.canlet.2004.07.049 Taverna, 2001, Methoxyamine potentiates DNA single strand breaks and double strand breaks induced by temozolomide in colon cancer cells, Mutat. Res., 485, 269, 10.1016/S0921-8777(01)00076-3 Taverna, 2003, Inhibition of base excision repair potentiates iododeoxyuridine-induced cytotoxicity and radiosensitization, Cancer Res., 63, 838 Taylor, 2000, A cell cycle-specific requirement for the XRCC1 BRCT II domain during mammalian DNA strand break repair, Mol. Cell. Biol., 20, 735, 10.1128/MCB.20.2.735-740.2000 Taylor, 2002, Central role for the XRCC1 BRCT I domain in mammalian DNA single-strand break repair, Mol. Cell. Biol., 22, 2556, 10.1128/MCB.22.8.2556-2563.2002 Tebbs, 1999, Requirement for the XRCC1 DNA base excision repair gene during early mouse development, Dev. Biol., 208, 513, 10.1006/dbio.1999.9232 Tell, 2005, The intracellular localization of APE1/Ref-1: more than a passive phenomenon?, Antioxid. Redox Signal., 7, 367, 10.1089/ars.2005.7.367 Tenesa, 2006, Association of MutYH and colorectal cancer, Br. J. Cancer, 95, 239, 10.1038/sj.bjc.6603239 Tentori, 2001, Combined effects of adenovirus-mediated wild-type p53 transduction, temozolomide and poly(ADP-ribose)polymerase inhibitor in mismatch repair deficient and non-proliferating tumor cells, Cell Death Differ., 8, 457, 10.1038/sj.cdd.4400832 Tentori, 2003, Systemic administration of GPI 15427, a novel poly(ADP-ribose)polymerase-1 inhibitor, increases the antitumor activity of temozolomide against intracranial melanoma, glioma, lymphoma, Clin. Cancer Res., 9, 5370 Tentori, 2006, Inhibition of poly(ADP-ribose)polymerase prevents irinotecan-induced intestinal damage and enhances irinotecan/temozolomide efficacy against colon carcinoma, FASEB J., 20, 1709, 10.1096/fj.06-5916fje Thompson, 2000, XRCC1 keeps DNA from getting stranded, Mutat. Res., 459, 1, 10.1016/S0921-8777(99)00058-0 Thompson, 1990, Molecular cloning of the human XRCC1 gene, which corrects defective DNA repair and sister chromatid exchange, Mol. Cell. Biol., 10, 6160, 10.1128/MCB.10.12.6160 Tomkinson, 1997, Mammalian DNA ligases, Bioessays, 19, 893, 10.1002/bies.950191009 Tomkinson, 1998, Structure and function of mammalian DNA ligases, Mutat. Res., 407, 1, 10.1016/S0921-8777(97)00050-5 Tomkinson, 2001, Completion of base excision repair by mammalian DNA ligases, Prog. Nucleic Acid Res. Mol. Biol., 68, 151, 10.1016/S0079-6603(01)68097-8 Trucco, 1998, DNA repair defect in poly(ADP-ribose)polymerase-deficient cell lines, Nucleic Acid Res., 26, 2644, 10.1093/nar/26.11.2644 Vaisman, 2000, The efficiency and fidelity of translesion synthesis past cisplatin and oxaliplatin GpG adducts by human DNA polymerase beta, J. Biol. Chem., 275, 13017, 10.1074/jbc.275.17.13017 Veuger, 2003, Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose)polymerase-1, Cancer Res., 63, 6008 Vidal, 2001, XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein–protein interactions, EMBO J., 20, 6530, 10.1093/emboj/20.22.6530 Waga, 1998, DNA replication fork in eukaryotic cells, Annu. Rev. Biochem., 67, 721, 10.1146/annurev.biochem.67.1.721 Wang, 1997, PARP is important for genomic stability but dispensable in apoptosis, Gene Dev., 11, 2347, 10.1101/gad.11.18.2347 Webster, 1992, Growth retardation and immunodeficiency in a patient with mutations in the DNA ligase I gene, Lancet, 339, 1508, 10.1016/0140-6736(92)91266-B Weinfeld, 2001, Complexities of BER, Prog. Nucleic Acid Res. Mol. Biol., 68, 125, 10.1016/S0079-6603(01)68094-2 Whitehouse, 2001, XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair, Cell, 104, 107, 10.1016/S0092-8674(01)00195-7 Wiebauer, 1990, 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, 5842, 10.1073/pnas.87.15.5842 Wiederhold, 2004, AP endonuclease-independent DNA base excision repair in human cells, Mol. Cell, 15, 209, 10.1016/j.molcel.2004.06.003 Wilson, 2001, The major human abasic endonuclease: formation, consequences and repair of abasic lesions in DNA, Mutat. Res., 485, 283, 10.1016/S0921-8777(01)00063-5 Wilson, 1996, Differential expression of the apurinic/apyrimidinic endonuclease (Ape/Ref-1) multifunctional DNA base excision repair gene during fetal development and in adult rat brain and testis, Mutat. Res., 362, 237, 10.1016/0921-8777(95)00053-4 Wu, 2004, Genome-wide identification of genes conferring resistance to the anticancer agents cisplatin, oxaliplatin, and mitomycin C, Cancer Res., 64, 3940, 10.1158/0008-5472.CAN-03-3113 Xanthoudakis, 1996, The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice, Proc. Natl. Acad. Sci. USA, 93, 8919, 10.1073/pnas.93.17.8919 Xie, 2004, Deficiencies in mouse MYH and OGG1 result in tumor predisposition and G to T mutations in codon 12 of the K-ras oncogene in lung tumors, Cancer Res., 64, 3096, 10.1158/0008-5472.CAN-03-3834 Zhang, 2005, DNA repair fidelity of base excision repair pathways in human cell extracts, DNA Repair (Amst.), 4, 263, 10.1016/j.dnarep.2004.10.004 Zhang, 2006, Germline mutations and polymorphic variants in MMR, E-cadherin and MYH genes associated with familial gastric cancer in Jiangsu of China, Int. J. Cancer, 119, 2592, 10.1002/ijc.22206 Zmudzka, 1988, Characterization of DNA polymerase beta mRNA: cell-cycle and growth response in cultured human cells, Nucleic Acid Res., 16, 9587, 10.1093/nar/16.20.9587