Base excision repair and lesion-dependent subpathways for repair of oxidative DNA damage

Antioxidants and Redox Signaling

Volumn 14, Issue 12, 2011, Pages 2491-2507

  Svilar, David ^a,b   Goellner, Eva M ^a,b   Almeida, Karen H ^c   Sobol, Robert W ^a,b,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c RHODE ISLAND COLLEGE   (United States)

^d UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXY 2' DEOXYCYTIDINE; 8 HYDROXYDEOXYGUANOSINE; CELL NUCLEUS DNA; DEOXYRIBONUCLEOSIDE; DNA GLYCOSYLTRANSFERASE; DNA POLYMERASE; GUANINE 2,6 DIAMINO 4 HYDROXY 5 FORMAMIDOPYRIMIDINE; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; EXCISION REPAIR; HUMAN; MAMMAL CELL; METABOLIC STRESS; NEOPLASM; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW;

DNA; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; HUMANS; MOLECULAR STRUCTURE; NEOPLASMS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES;

MAMMALIA;

EID: 79957456954     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2010.3466     Document Type: Review

References (100)

1. Akbari M, Solvang-Garten K, Hanssen-Bauer A, Lieske NV, Pettersen HS, Pettersen GK, Wilson DM 3rd, Krokan HE, and Otterlei M. Direct interaction between XRCC1 and UNG2 facilitates rapid repair of uracil in DNA by XRCC1 complexes. DNA Repair (Amst) 9: 785-795, 2010.
2. Albright CD, Salganik RI, Craciunescu CN, Mar MH, and Zeisel SH. Mitochondrial and microsomal derived reactive oxygen species mediate apoptosis induced by transforming growth factor-beta1 in immortalized rat hepatocytes. J Cell Biochem 89: 254-261, 2003. (Pubitemid 36547260)
3. Almeida KH and Sobol RW. A unified view of base excision repair: lesion-dependent protein complexes regulated by post-translational modification. DNA Repair 6: 695-711, 2007. (Pubitemid 46670095)
4. Almeida KH and Sobol RW. Increased specificity and ef-ficiency of base excision repair through complex formation. In: DNA Damage Recognition. Edited by Siede W, Doetsch PW, and Kow YW. New York: Marcel Dekker, 2005, pp. 33-64.
5. BartschHandNair J.Oxidative stress and lipid peroxidationderived DNA-lesions in inflammation driven carcinogenesis. Cancer Detect Prevent 28: 385-391, 2004.
6. Belousova EA, Maga G, Fan Y, Kubareva EA, Romanova EA, Lebedeva NA, Oretskaya TS, and Lavrik OI. DNA polymerases beta and lambda bypass thymine glycol in gapped DNA structures. Biochemistry 49: 4695-4704, 2010.
7. Bessho T, Roy R, Yamamoto K, Kasai H, Nishimura S, Tano K, and Mitra S. Repair of 8-hydroxyguanine in DNA by mammalian N-methylpurine-DNA glycosylase. Proc Natl Acad Sci USA 90: 8901-8904, 1993. (Pubitemid 23306418)
8. Bhakat KK, Hazra TK, and Mitra S. Acetylation of the human DNA glycosylase NEIL2 and inhibition of its activity. Nucleic Acids Res 32: 3033-3039, 2004. (Pubitemid 39022994)
9. Bjelland S and Seeberg E. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 531: 37-80, 2003. (Pubitemid 37456723)
10. Boorstein RJ, Cummings A Jr, Marenstein DR, Chan MK, Ma Y, Neubert TA, Brown SM, and Teebor GW. Definitive identification of mammalian 5-hydroxymethyluracil DNA N-glycosylase activity as SMUG1. J Biol Chem 276: 41991-41997, 2001.
11. Campalans A, Marsin S, Nakabeppu Y, O'Connor T R, Boiteux S, and Radicella JP. XRCC1 interactions with multiple DNA glycosylases: a model for its recruitment to base excision repair. DNA Repair (Amst) 4: 826-835, 2005. (Pubitemid 40835854)
12. Cannon SV, Cummings A, and Teebor GW. 5-Hydroxymethylcytosine DNA glycosylase activity in mammalian tissue. Biochem Biophys ResCommun 51: 1173-1179, 1988. (Pubitemid 18095244)
13. Cheadle JP and Sampson JR. Exposing the MYtH about base excision repair and human inherited disease. Hum Mol Genet 12: R159-R165, 2003. (Pubitemid 37259328)
14. Chetsanga CJ and Grigorian C. A dose-response study on opening of imidazole ring of adenine in DNA by ionizing radiation. Int J Radiat Biol Relat Stud Phys Chem Med 44: 321-331, 1983. (Pubitemid 14226877)
15. Cooke MS, Loft S, Olinski R, Evans MD, Bialkowski K, Wagner JR, Dedon PC, Moller P, Greenberg MM, and Cadet J. Recommendations for standardized description of and nomenclature concerning oxidatively damaged nucleobases in DNA. Chem Res Toxicol 23: 705-707, 2010.
16. D'Errico M, Parlanti E, and Dogliotti E. Mechanism of oxidative DNA damage repair and relevance to human pathology. Mutat Res 659: 4-14, 2008.
17. Dang CV, Le A, and Gao P. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clin Cancer Res 15: 6479-6483, 2009.
18. Darwanto A, Theruvathu JA, Sowers JL, Rogstad DK, Pascal T, Goddard W 3rd, and Sowers LC. Mechanisms of base selection by human single-stranded selective monofunctional uracil-DNA glycosylase. J Biol Chem 284: 15835-15846, 2009.
19. Das A, Wiederhold L, Leppard JB, Kedar P, Prasad R, Wang H, Boldogh I, Karimi-Busheri F, Weinfeld M, Tomkinson AE, Wilson SH, Mitra S, and Hazra TK. NEIL2-initiated, APE-independent repair of oxidized bases in DNA: evidence for a repair complex in human cells. DNA Repair (Amst) 5: 1439-1448, 2006. (Pubitemid 44768083)
20. David SS, O'Shea VL, and Kundu S. Base-excision repair of oxidative DNA damage. Nature 447: 941-950, 2007. (Pubitemid 46975761)
21. DeMott MS, Beyret E, Wong D, Bales BC, Hwang JT, Greenberg MM, and Demple B. Covalent trapping of human DNA polymerase beta by the oxidative DNA lesion 2-deoxyribonolactone. J Biol Chem 277: 7637-7640, 2002. (Pubitemid 34968206)
22. Dizdaroglu M, Karakaya A, Jaruga P, Slupphaug G, and Krokan H. Novel activities of human uracil DNA Nglycosylase for cytosine-derived products of oxidative DNA damage. Nucleic Acids Res 24: 418-422, 1996.
23. Dizdaroglu M, Kirkali G, and Jaruga P. Formamidopyrimidines in DNA: mechanisms of formation, repair, and biological effects. Free Radic Biol Med 45: 1610-1621, 2008.
24. DNA Repair Database. DNA repair database from 7 organisms. http:==dnapittcrew.upmc.com . Accessed, 2010.
25. Dosanjh MK, Chenna A, Kim E, Fraenkel-Conrat H, Samson L, and Singer B. All four known cyclic adducts formed in DNA by the vinyl chloride metabolite chloroacetaldehyde are released by a human DNA glycosylase. Proc Natl Acad Sci USA 91: 1024-1028, 1994. (Pubitemid 24048501)
26. Dosanjh MK, Roy R, Mitra S, and Singer B. 1,N6-ethenoadenine is preferred over 3-methyladenine as substrate by a cloned human N-methylpurine-DNA glycosylase (3-methyladenine-DNA glycosylase). Biochemistry 33: 1624-1628, 1994.
27. Feig DI, Sowers LC, and Loeb LA. Reverse chemical mutagenesis: identification of the mutagenic lesions resulting from reactive oxygen species-mediated damage to DNA. Proc Natl Acad Sci USA 91: 6609-6613, 1994. (Pubitemid 24200711)
28. Fischhaber PL, Gerlach VL, Feaver WJ, Hatahet Z, Wallace SS, and Friedberg EC. Human DNA polymerase kappa bypasses and extends beyond thymine glycols during translesion synthesis in vitro, preferentially incorporating correct nucleotides. J Biol Chem 277: 37604-37611, 2002.
29. Frenkel K, Goldstein MS, Duker NJ, and Teebor GW. Identification of the cis-thymine glycol moiety in oxidized deoxyribonucleic acid. Biochemistry 20: 750-754, 1981.
30. Friedberg EC, Walker GC, Siede W, Wood RD, Schultz RA, and Ellenberger T. DNA Repair and Mutagenesis. 2nd Ed. Washington, DC: ASM Press, 2006, p. 164.
31. Grin IR, Dianov GL, and Zharkov DO. The role of mammalian NEIL1 protein in the repair of 8-oxo-7,8-dihydroadenine in DNA. FEBS Lett 584: 1553-1557, 2010.
32. Gros L, Ishchenko AA, and Saparbaev M. Enzymology of repair of etheno-adducts. Mutat Res 531: 219-229, 2003. (Pubitemid 37456734)
33. Gros L, Maksimenko AV, Privezentzev CV, Laval J, and Saparbaev MK. Hijacking of the human alkyl-N-purine-DNA glycosylase by 3,N4-ethenocytosine, a lipid peroxidationinduced DNA adduct. J Biol Chem 279: 17723-17730, 2004. (Pubitemid 38560538)
34. Guan L and Greenberg MM. Irreversible inhibition of DNA polymerase beta by an oxidized abasic lesion. J Am Chem Soc 132: 5004-5005, 2010.
35. Hailer MK, Slade PG, Martin BD, Rosenquist TA, and Sugden KD. Recognition of the oxidized lesions spiroiminodihydantoin and guanidinohydantoin in DNA by the mammalian base excision repair glycosylases NEIL1 and NEIL2. DNA Repair (Amst) 4: 41-50, 2005. (Pubitemid 39469081)
36. Hanes JW, Thal DM, and Johnson KA. Incorporation and replication of 8-oxo-deoxyguanosine by the human mitochondrial DNA polymerase. J Biol Chem 281: 36241-36248, 2006. (Pubitemid 46041359)
37. Hansen AB, Griner NB, Anderson JP, Kujoth GC, Prolla TA, Loeb LA, and Glick E. Mitochondrial DNA integrity is not dependent on DNA polymerase-beta activity. DNA Repair (Amst) 5: 71-79, 2006. (Pubitemid 41832513)
38. Hardeland U, Bentele M, Jiricny J, and Schar P. The versatile thymine DNA-glycosylase: a comparative characterization of the human, Drosophila and fission yeast orthologs. Nucleic Acids Res 31: 2261-2271, 2003. (Pubitemid 37442093)
39. Harris JL, Jakob B, Taucher-Scholz G, Dianov GL, Becherel OJ, and Lavin MF. Aprataxin, poly-ADP ribose polymerase 1 (PARP-1) and apurinic endonuclease 1 (APE1) function together to protect the genome against oxidative damage. Hum Mol Genet 8: 4102-4117, 2009.
40. Hashimoto K, Tominaga Y, Nakabeppu Y, and Moriya M. Futile short-patch DNA base excision repair of adenine:8-oxoguanine mispair. Nucleic Acids Res 32: 5928-5934, 2004. (Pubitemid 39619174)
41. Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med 361: 1475-1485, 2009.
42. Jaruga P, Xiao Y, Vartanian V, Lloyd RS, and Dizdaroglu M. Evidence for the involvement of DNA repair enzyme NEIL1 in nucleotide excision repair of (50R)-and (50S)-8,50-cyclo-20-deoxyadenosines. Biochemistry 49: 1053-1055, 2010.
43. Jensen A, Calvayrac G, Karahalil B, Bohr VA, and Stevnsner T. Mammalian 8-oxoguanine DNA glycosylase 1 incises 8-oxoadenine opposite cytosine in nuclei and mitochondria, while a different glycosylase incises 8-oxoadenine opposite guanine in nuclei. J Biol Chem 278: 19541-19548, 2003. (Pubitemid 36799352)
44. Jovanovic SV and Simic MG. Mechanism of OH radical reaction with thymine and uracil derivatives. J Am Chem Soc 108: 5968-5972, 1986. (Pubitemid 16023962)
45. Kalam MA, Haraguchi K, Chandani S, Loechler EL, Moriya M, Greenberg MM, and Basu AK. Genetic effects of oxidative DNA damages: comparative mutagenesis of the imidazole ring-opened formamidopyrimidines (Fapy lesions) and 8-oxo-purines in simian kidney cells. Nucleic Acids Res 34: 2305-2315, 2006. (Pubitemid 43985668)
46. Kalivendi SV, Kotamraju S, Cunningham S, Shang T, Hillard CJ, and Kalyanaraman B. 1-Methyl-4-phenylpyridinium (MPP\+)-induced apoptosis and mitochondrial oxidant generation: role of transferrin-receptor-dependent iron and hydrogen peroxide. Biochem J 371: 151-164, 2003. (Pubitemid 36458089)
47. Kasai H and Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res 12: 2137-2145, 1984.
48. Krahn JM, Beard WA, Miller H, Grollman AP, and Wilson SH. Structure of DNA polymerase beta with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential. Structure 1: 121-127, 2003. (Pubitemid 36071499)
49. Kriaucionis S and Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930, 2009.
50. Kusumoto R, Masutani C, Iwai S, and Hanaoka F. Translesion synthesis by human DNA polymerase eta across thymine glycol lesions. Biochemistry 41: 6090-6099, 2002. (Pubitemid 34498915)
51. LeDoux SP, Druzhyna NM, Hollensworth SB, Harrison JF, and Wilson GL. Mitochondrial DNA repair: a critical player in the response of cells of the CNS to genotoxic insults. Neuroscience 145: 1249-1259, 2007. (Pubitemid 46604848)
52. LeDoux SP, Wilson GL, Beecham EJ, Stevnsner T, Wassermann K, and Bohr VA. Repair of mitochondrial DNA after various types of DNA damage in Chinese hamster ovary cells. Carcinogenesis 13: 1967-1973, 1992.
53. Lee CY, Delaney JC, Kartalou M, Lingaraju GM, Maor-Shoshani A, Essigmann JM, and Samson LD. Recognition and processing of a new repertoire of DNA substrates by human 3-methyladenine DNA glycosylase (AAG). Biochemistry 48: 1850-1861, 2009.
54. Lee DH and Pfeifer GP. Translesion synthesis of 7,8-dihydro-8-oxo-20- deoxyguanosine by DNA polymerase eta in vivo. Mutat Res 641: 19-26, 2008.
55. Liu M, Bandaru V, Bond JP, Jaruga P, Zhao X, Christov PP, Burrows CJ, Rizzo CJ, Dizdaroglu M, and Wallace SS. The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo. Proc Natl Acad Sci USA 107: 4925-4930, 2010.
56. Longley MJ, Prasad R, Srivastava DK, Wilson SH, and Copeland WC. Identification of 50-deoxyribose phosphate lyase activity in human DNA polymerase and its role in mitochondrial base excision repair in vitro. Proc Natl Acad Sci USA 95: 12244-12248, 1988.
57. Maga G, Crespan E, Wimmer U, van Loon B, Amoroso A, Mondello C, Belgiovine C, Ferrari E, Locatelli G, Villani G, and Hubscher U. Replication protein A and proliferating cell nuclear antigen coordinate DNA polymerase selection in 8-oxo-guanine repair. Proc Natl Acad Sci USA 105: 20689-20694, 2008.
58. Maga G, Villani G, Crespan E, Wimmer U, Ferrari E, Bertocci B, and Hubscher U. 8-Oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447: 606-608, 2007. (Pubitemid 46868042)
59. Mandavilli BS, Santos JH, and Van Houten B. Mitochondrial DNA repair and aging. Mutat Res 509: 127-151, 2002. (Pubitemid 35341457)
60. Marenstein DR, Chan MK, Altamirano A, Basu AK, Boorstein RJ, Cunningham RP, and Teebor GW. Substrate specificity of human endonuclease III (hNTH1): effect of human APE1 on hNTH1 activity. J Biol Chem 278: 9005-9012, 2003. (Pubitemid 36800378)
61. Marnett LJ. Oxy radicals, lipid peroxidation and DNA damage. Toxicology 181-182: 219-222, 2002. (Pubitemid 36015702)
62. Marnett LJ. Oxyradicals and DNA damage. Carcinogenesis 21: 361-370, 2000. (Pubitemid 30137921)
63. Martin KR and Barrett JC. Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity. Hum Exp Toxicol 21: 71-75, 2002. (Pubitemid 34591267)
64. Masaoka A, Matsubara M, Hasegawa R, Tanaka T, Kurisu S, Terato H, Ohyama Y, Karino N, Matsuda A, and Ide H. Mammalian 5-formyluracil-DNA glycosylase, 2: role of SMUG1 uracil-DNA glycosylase in repair of 5-formyluracil and other oxidized and deaminated base lesions. Biochemistry 42:5003-5012, 2003. (Pubitemid 36532054)
65. Matsumoto Y, Zhang QM, Takao M, Yasui A, and Yonei S. Escherichia coli Nth and human hNTH1 DNA glycosylases are involved in removal of 8-oxoguanine from 8-oxoguanine=guanine mispairs in DNA. Nucleic Acids Res 29: 1975-1981, 2001. (Pubitemid 32433283)
66. McCarthy S, Somayajulu M, Sikorska M, Borowy-Borowski H, and Pandey S. Paraquat induces oxidative stress and neuronal cell death; neuroprotection by water-soluble Coenzyme Q10. Toxicol Appl Pharmacol 201: 21-31, 2004 . (Pubitemid 39446323)
67. Nakabeppu Y, Kajitani K, Sakamoto K, Yamaguchi H, and Tsuchimoto D. MTH1, an oxidized purine nucleoside triphosphatase, prevents the cytotoxicity and neurotoxicity of oxidized purine nucleotides. DNA Repair (Amst) 5: 761-772, 2006. (Pubitemid 43928881)
68. Nazarkina ZK, Khodyreva SN, Marsin S, Radicella JP, and Lavrik OI. Study of interaction of XRCC1 with DNA and proteins of base excision repair by photoaffinity labeling technique. Biochemistry (Mosc) 72: 878-886, 2007. (Pubitemid 47366850)
69. Neeley WL and Essigmann JM. Mechanisms of formation, genotoxicity, and mutation of guanine oxidation products. Chem Res Toxicol 19: 491-505, 2006.
70. Oka S, Ohno M, Tsuchimoto D, Sakumi K, Furuichi M, and Nakabeppu Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J 27: 421-432, 2008. (Pubitemid 351161663)
71. Olinski R, Zastawny T, Budzbon J, Skokowski J, Zegarski W, and Dizdaroglu M. DNA base modifications in chromatin of human cancerous tissues. FEBS Lett 309: 193-198, 1992.
72. Parker AR, Sieber OM, Shi C, Hua L, Takao M, Tomlinson IP, and Eshleman JR. Cells with pathogenic biallelic mutations in the human MUTYH gene are defective in DNA damage binding and repair. Carcinogenesis 26: 2010-2018, 2005. (Pubitemid 41631275)
73. Perillo B, Ombra MN, Bertoni A, Cuozzo C, Sacchetti S, Sasso A, Chiariotti L, Malorni A, Abbondanza C, and Avvedimento EV. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science 319: 202-206, 2008.
74. Phosphosite. 2010. PhosphositePlus. http:==www.phos phosite.org .
75. Roberts SA, Strande N, Burkhalter MD, Strom C, Havener JM, Hasty P, and Ramsden DA. Ku is a 50-dRP=AP lyase that excises nucleotide damage near broken ends. Nature 464: 1214-1217, 2010.
76. Rossi MN, Carbone M, Mostocotto C, Mancone C, Tripodi M, Maione R, and Amati P. Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J Biol Chem 284: 31616-31624, 2009.
77. Rydberg B, Qiu ZH, Dosanjh MK, and Singer B. Partial purification of a human DNA glycosylase acting on the cyclic carcinogen adduct 1,N6-ethenodeoxyadenosine. Cancer Res 52: 1377-1379, 1992.
78. Saparbaev M, Langouet S, Privezentzev CV, Guengerich FP, Cai H, Elder RH, and Laval J. 1,N(2)-ethenoguanine, a mutagenic DNA adduct, is a primary substrate of Escherichia coli mismatch-specific uracil-DNA glycosylase and human alkylpurine-DNA-N-glycosylase. J Biol Chem 277: 26987-26993, 2002. (Pubitemid 34951710)
79. Singer B, Antoccia A, Basu AK, Dosanjh MK, Fraenkel-Conrat H, Gallagher PE,Kusmierek JT, Qiu ZH, and Rydberg B. Both purified human 1,N6-ethenoadenine- binding protein and purified human 3-methyladenine-DNA glycosylase act on 1,N6-ethenoadenine and 3-methyladenine. Proc Natl Acad Sci USA 89: 9386-9390, 1992.
80. Sobol RW, Horton JK, Kuhn R, Gu H, Singhal RK, Prasad R, Rajewsky K, and Wilson SH. Requirement of mammalian DNA polymerase-ß in base-excision repair. Nature 379: 183-186, 1996. (Pubitemid 26020204)
81. Sung JS, DeMott MS, and Demple B. Long-patch base excision DNA repair of 2-deoxyribonolactone prevents the formation of DNA-protein cross-links with DNA polymerase beta. J Biol Chem 280: 39095-39103, 2005. (Pubitemid 41713860)
82. Szczesny B, Tann AW, Longley MJ, Copeland WC, and Mitra S. Long patch base excision repair in mammalian mitochondrial genomes. J Biol Chem 283: 26349-26356, 2008.
83. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, and Rao A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935, 2009.
84. Takata K, Shimizu T, Iwai S, and Wood RD. Human DNA polymerase N (POLN) is a low fidelity enzyme capable of error-free bypass of 5S-thymine glycol. J Biol Chem 281: 23445-23455, 2006. (Pubitemid 44274119)
85. Tan X, Grollman AP, and Shibutani S. Comparison of the mutagenic properties of 8-oxo-7,8-dihydro-20-deoxyadenosine and 8-oxo-7,8-dihydro-20- deoxyguanosineDNAlesions in mammalian cells. Carcinogenesis 20: 2287-2292, 1999. (Pubitemid 30015900)
86. Tang J, Goellner EM, Wang XW, Trivedi RN, St Croix CM, Jelezcova E, Svilar D, Brown AR, and Sobol RW. Bioenergetic metabolites regulate base excision repair-dependent cell death in response to DNA damage. Mol Cancer Res 8: 67-79, 2010.
87. Tardy-Planechaud S, Fujimoto J, Lin SS, and Sowers LC. Solid phase synthesis and restriction endonuclease cleavage of oligodeoxynucleotides containing 5-(hydroxymethyl)-cytosine. Nucleic Acids Res 25: 553-559, 1997.
88. Vallyathan V and Shi X. The role of oxygen free radicals in occupational and environmental lung diseases. Environ Health Perspect 105(suppl 1): 165-177, 1997. (Pubitemid 27168292)
89. Wallace SS. AP endonucleases and DNA glycosylases that recognize oxidative DNA damage. Environ Mol Mutagen 12: 431-477, 1988. (Pubitemid 19246987)
90. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, Joseph J, Lopez M, Kalyanaraman B, Mutlu GM, Budinger GR, and Chandel NS. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci USA 107: 8788-8793, 2010.
91. Wibley JE, Waters TR, Haushalter K, Verdine GL, and Pearl LH. Structure and specificity of the vertebrate anti-mutator uracil-DNA glycosylase SMUG1. Mol Cell 1: 1647-1659, 2003. (Pubitemid 36776549)
92. Wiederhold L, Leppard JB, Kedar P, Karimi-Busheri F, Rasouli-Nia A, Weinfeld M, Tomkinson AE, Izumi T, Prasad R, Wilson SH, Mitra S, and Hazra TK. AP endonucleaseindependent DNA base excision repair in human cells. Mol Cell 15: 209-220, 2004. (Pubitemid 38950968)
93. Wong RS, Sczepanski JT, and Greenberg MM. Excision of a lyase-resistant oxidized abasic lesion from DNA. Chem Res Toxicol 23: 766-770, 2010.
94. Wood RD, Mitchell M, Sgouros J, and Lindahl T. Human DNA repair genes. Science 291: 1284-1289, 2001. (Pubitemid 32173086)
95. Yakes FM and Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA 94: 514-519, 1997. (Pubitemid 27053665)
96. Yoon JH, Iwai S, O'Connor TR, and Pfeifer GP. Human thymine DNA glycosylase (TDG) and methyl-CpG-binding protein 4 (MBD4) excise thymine glycol (Tg) from a Tg:G mispair. Nucleic Acids Res 31: 5399-5404, 2003. (Pubitemid 37441908)
97. Zhang Y, Yuan F, Wu X, Taylor JS, and Wang Z. Response of human DNA polymerase iota to DNA lesions. Nucleic Acids Res 29: 928-935, 2001. (Pubitemid 32162261)
98. Zhang Y, Yuan F, Wu X, Wang M, Rechkoblit O, Taylor JS, Geacintov NE, and Wang Z. Error-free and error-prone lesion bypass by human DNA polymerase kappa in vitro. Nucleic Acids Res 28: 4138-4146, 2000.
99. Zheng L, Zhou M, Guo Z, Lu H, Qian L, Dai H, Qiu J, Yakubovskaya E, Bogenhagen DF, Demple B, and Shen B. Human DNA2 is a mitochondrial nuclease=helicase for efficient processing of DNA replication and repair intermediates. Mol Cell 32: 325-336, 2008.
100. Zorov DB, Juhaszova M, and Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 1757: 509-517, 2006.