Oxidized base damage and single-strand break repair in mammalian genomes: Role of disordered regions and posttranslational modifications in early enzymes

Progress in Molecular Biology and Translational Science

Volumn 110, Issue , 2012, Pages 123-153

  Hegde, Muralidhar L ^a   Izumi, Tadahide ^b   Mitra, Sankar ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Base excision repair; Disordered terminal segments; DNA glycosylases; End processing proteins; Posttranslational modifications; Reactive oxygen species; Repair complexes; Single strand breaks

Indexed keywords

EID: 84862978423     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-387665-2.00006-7     Document Type: Chapter

References (195)

1. T.L. Dawson, G.J. Gores, A.L. Nieminen, B. Herman, and J.J. Lemasters Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes Am J Physiol 264 1993 C961 C967
2. K.K. Griendling, D. Sorescu, and M. Ushio-Fukai NAD(P)H oxidase: role in cardiovascular biology and disease Circ Res 86 2000 494 501 (Pubitemid 30165039)
3. T. Lindahl Instability and decay of the primary structure of DNA Nature 362 1993 709 715 (Pubitemid 23125973)
4. S. Mitra, M.L. Hegde, C.A. Theriot, A. Das, P.M. Hegde, and T.K. Hazra Complexity in repair of oxidative genome damage and its regulation Proceedings of princess Takamatsu symposium, Tokyo, Japan 2009
5. J.M. Di Noia, and M.S. Neuberger Molecular mechanisms of antibody somatic hypermutation Annu Rev Biochem 76 2007 1 22
6. B. Doseth, T. Visnes, A. Wallenius, I. Ericsson, A. Sarno, and H.S. Pettersen Uracil-DNA glycosylase in base excision repair and adaptive immunity: species differences between man and mouse J Biol Chem 286 2011 16669 16680
7. M. Dizdaroglu Base-excision repair of oxidative DNA damage by DNA glycosylases Mutat Res 591 2005 45 59 (Pubitemid 41654839)
8. M.L. Hegde, T.K. Hazra, and S. Mitra Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells Cell Res 18 2008 27 47
9. S. Mitra, T. Izumi, I. Boldogh, K.K. Bhakat, J.W. Hill, and T.K. Hazra Choreography of oxidative damage repair in mammalian genomes Free Radic Biol Med 33 2002 15 28 (Pubitemid 34681002)
10. M.L. Dodson, and R.S. Lloyd Mechanistic comparisons among base excision repair glycosylases Free Radic Biol Med 32 2002 678 682 (Pubitemid 34286588)
11. L. Wiederhold, J.B. Leppard, P. Kedar, F. Karimi-Busheri, A. Rasouli-Nia, and M. Weinfeld AP endonuclease-independent DNA base excision repair in human cells Mol Cell 15 2004 209 220 (Pubitemid 38950968)
12. G.A. Hildrestrand, C.G. Neurauter, D.B. Diep, C.G. Castellanos, S. Krauss, and M. Bjoras Expression patterns of Neil3 during embryonic brain development and neoplasia BMC Neurosci 10 2009 45
13. M. Takao, Y. Oohata, K. Kitadokoro, K. Kobayashi, S. Iwai, and A. Yasui Human Nei-like protein NEIL3 has AP lyase activity specific for single-stranded DNA and confers oxidative stress resistance in Escherichia coli mutant Genes cells 14 2009 261 270
14. M.T. Russo, G. De Luca, P. Degan, and M. Bignami Different DNA repair strategies to combat the threat from 8-oxoguanine Mutat Res 614 2007 69 76 (Pubitemid 44909210)
15. R.W. Sobol, R. Prasad, A. Evenski, A. Baker, X.P. Yang, and J.K. Horton The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity Nature 405 2000 807 810 (Pubitemid 30407855)
16. G. Frosina, P. Fortini, O. Rossi, F. Carrozzino, G. Raspaglio, and L.S. Cox Two pathways for base excision repair in mammalian cells J Biol Chem 271 1996 9573 9578 (Pubitemid 26137362)
17. Y. Liu, H.I. Kao, and R.A. Bambara Flap endonuclease 1: a central component of DNA metabolism Annu Rev Biochem 73 2004 589 615 (Pubitemid 39050381)
18. L. Zheng, M. Zhou, Z. Guo, H. Lu, L. Qian, and H. Dai Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates Mol Cell 32 2008 325 336
19. J.P. Duxin, B. Dao, P. Martinsson, N. Rajala, L. Guittat, and J.L. Campbell Human Dna2 is a nuclear and mitochondrial DNA maintenance protein Mol Cell Biol 29 2009 4274 4282
20. R. Prasad, G.L. Dianov, V.A. Bohr, and S.H. Wilson FEN1 stimulation of DNA polymerase beta mediates an excision step in mammalian long patch base excision repair J Biol Chem 275 2000 4460 4466 (Pubitemid 30094690)
21. A.J. Podlutsky, I.I. Dianova, V.N. Podust, V.A. Bohr, and G.L. Dianov Human DNA polymerase beta initiates DNA synthesis during long-patch repair of reduced AP sites in DNA EMBO J 20 2001 1477 1482 (Pubitemid 32233987)
22. A. Klungland, and T. Lindahl Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1) EMBO J 16 1997 3341 3348 (Pubitemid 27234971)
23. Y. Matsumoto, K. Kim, J. Hurwitz, R. Gary, D.S. Levin, and A.E. Tomkinson Reconstitution of proliferating cell nuclear antigen-dependent repair of apurinic/apyrimidinic sites with purified human proteins J Biol Chem 274 1999 33703 33708 (Pubitemid 129511685)
24. Y. Matsumoto, and K. Kim Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair Science 269 1995 699 702
25. T. Ellenberger, and A.E. Tomkinson Eukaryotic DNA ligases: structural and functional insights Annu Rev Biochem 77 2008 313 338
26. C.F. Kuo, D.E. McRee, C.L. Fisher, S.F. O'Handley, R.P. Cunningham, and J.A. Tainer Atomic structure of the DNA repair [4Fe-4S] enzyme endonuclease III Science 258 1992 434 440
27. M.M. Thayer, H. Ahern, D. Xing, R.P. Cunningham, and J.A. Tainer Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure EMBO J 14 1995 4108 4120
28. A. Das, L. Rajagopalan, V.S. Mathura, S.J. Rigby, S. Mitra, and T.K. Hazra Identification of a zinc finger domain in the human NEIL2 (Nei-like-2) protein J Biol Chem 279 2004 47132 47138 (Pubitemid 39518370)
29. J.B. Parker, M.A. Bianchet, D.J. Krosky, J.I. Friedman, L.M. Amzel, and J.T. Stivers Enzymatic capture of an extrahelical thymine in the search for uracil in DNA Nature 449 2007 433 437 (Pubitemid 47509542)
30. G. Slupphaug, C.D. Mol, B. Kavli, A.S. Arvai, H.E. Krokan, and J.A. Tainer A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA Nature 384 1996 87 92 (Pubitemid 26374594)
31. H.E. Krokan, H. Nilsen, F. Skorpen, M. Otterlei, and G. Slupphaug Base excision repair of DNA in mammalian cells FEBS Lett 476 2000 73 77 (Pubitemid 30394654)
32. A. Das, L. Wiederhold, J.B. Leppard, P. Kedar, R. Prasad, and H. Wang NEIL2-initiated, APE-independent repair of oxidized bases in DNA: evidence for a repair complex in human cells DNA Repair (Amst) 5 2006 1439 1448 (Pubitemid 44768083)
33. T.K. Hazra, T. Izumi, I. Boldogh, B. Imhoff, Y.W. Kow, and P. Jaruga Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA Proc Natl Acad Sci USA 99 2002 3523 3528 (Pubitemid 34252141)
34. T.K. Hazra, Y.W. Kow, Z. Hatahet, B. Imhoff, I. Boldogh, and S.K. Mokkapati Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions J Biol Chem 277 2002 30417 30420 (Pubitemid 34970730)
35. T. Izumi, L.R. Wiederhold, G. Roy, R. Roy, A. Jaiswal, and K.K. Bhakat Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage Toxicology 193 2003 43 65 (Pubitemid 37340143)
36. M. Awada, and P.C. Dedon Formation of the 1, N2-glyoxal adduct of deoxyguanosine by phosphoglycolaldehyde, a product of 3′-deoxyribose oxidation in DNA Chem Res Toxicol 14 2001 1247 1253 (Pubitemid 32911463)
37. J.L. Parsons, I.I. Dianova, and G.L. Dianov APE1 is the major 3′-phosphoglycolate activity in human cell extracts Nucleic Acids Res 32 2004 3531 3536 (Pubitemid 39157703)
38. T. Zhou, K. Akopiants, S. Mohapatra, P.S. Lin, K. Valerie, and D.A. Ramsden Tyrosyl-DNA phosphodiesterase and the repair of 3′- phosphoglycolate-terminated DNA double-strand breaks DNA Repair (Amst) 8 2009 901 911
39. S.F. El-Khamisy, G.M. Saifi, M. Weinfeld, F. Johansson, T. Helleday, and J.R. Lupski Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1 Nature 434 2005 108 113 (Pubitemid 40349394)
40. J.J. Pouliot, K.C. Yao, C.A. Robertson, and H.A. Nash Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes Science 286 1999 552 555
41. S.W. Yang, A.B. Burgin Jr., B.N. Huizenga, C.A. Robertson, K.C. Yao, and H.A. Nash A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases Proc Natl Acad Sci USA 93 1996 11534 11539 (Pubitemid 26347156)
42. M. Weinfeld, R.S. Mani, I. Abdou, R.D. Aceytuno, and J.N. Glover Tidying up loose ends: the role of polynucleotide kinase/phosphatase in DNA strand break repair Trends Biochem Sci 36 2011 262 271
43. I. Ahel, U. Rass, S.F. El-Khamisy, S. Katyal, P.M. Clements, and P.J. McKinnon The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates Nature 443 2006 713 716 (Pubitemid 44564716)
44. K.W. Caldecott Mammalian single-strand break repair: mechanisms and links with chromatin DNA Repair (Amst) 6 2007 443 453 (Pubitemid 46357048)
45. S.N. Guzder, C. Torres-Ramos, R.E. Johnson, L. Haracska, L. Prakash, and S. Prakash Requirement of yeast Rad1-Rad10 nuclease for the removal of 3′-blocked termini from DNA strand breaks induced by reactive oxygen species Genes Dev 18 2004 2283 2291 (Pubitemid 39209576)
46. M. Masson, C. Niedergang, V. Schreiber, S. Muller, J. Menissier-de Murcia, and G. de Murcia XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage Mol Cell Biol 18 1998 3563 3571 (Pubitemid 28240528)
47. L. Lan, S. Nakajima, Y. Oohata, M. Takao, S. Okano, and M. Masutani In situ analysis of repair processes for oxidative DNA damage in mammalian cells Proc Natl Acad Sci USA 101 2004 13738 13743 (Pubitemid 39298477)
48. P.O. Hassa, and M.O. Hottiger The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases Front Biosci 13 2008 3046 3082 (Pubitemid 351589219)
49. R. Krishnakumar, and W.L. Kraus The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets Mol Cell 39 2010 8 24
50. C. Boehler, L.R. Gauthier, O. Mortusewicz, D.S. Biard, J.M. Saliou, and A. Bresson Poly(ADP-ribose) polymerase 3 (PARP3), a newcomer in cellular response to DNA damage and mitotic progression Proc Natl Acad Sci USA 108 2011 2783 2788
51. A.E. Fisher, H. Hochegger, S. Takeda, and K.W. Caldecott Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase Mol Cell Biol 27 2007 5597 5605 (Pubitemid 47124411)
52. M. Rouleau, A. Patel, M.J. Hendzel, S.H. Kaufmann, and G.G. Poirier PARP inhibition: PARP1 and beyond Nat Rev Cancer 10 2010 293 301
53. V. Schreiber, F. Dantzer, J.C. Ame, and G. de Murcia Poly(ADP-ribose): novel functions for an old molecule Nat Rev Mol Cell Biol 7 2006 517 528 (Pubitemid 44036457)
54. S.L. Rulten, A.E. Fisher, I. Robert, M.C. Zuma, M. Rouleau, and L. Ju PARP-3 and APLF function together to accelerate nonhomologous end-joining Mol Cell 41 2011 33 45
55. M. Akbari, T. Visnes, H.E. Krokan, and M. Otterlei Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis DNA Repair (Amst) 7 2008 605 616
56. V.A. Bohr Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells Free Radic Biol Med 32 2002 804 812 (Pubitemid 34439251)
57. B. Szczesny, A.W. Tann, M.J. Longley, W.C. Copeland, and S. Mitra Long patch base excision repair in mammalian mitochondrial genomes J Biol Chem 283 2008 26349 26356
58. K. Hashiguchi, J.A. Stuart, N.C. de Souza-Pinto, and V.A. Bohr The C-terminal alphaO helix of human Ogg1 is essential for 8-oxoguanine DNA glycosylase activity: the mitochondrial beta-Ogg1 lacks this domain and does not have glycosylase activity Nucleic Acids Res 32 2004 5596 5608 (Pubitemid 39545676)
59. J. Hu, N.C. de Souza-Pinto, K. Haraguchi, B.A. Hogue, P. Jaruga, and M.M. Greenberg Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes J Biol Chem 280 2005 40544 40551 (Pubitemid 41780543)
60. B. Karahalil, N.C. de Souza-Pinto, J.L. Parsons, R.H. Elder, and V.A. Bohr Compromised incision of oxidized pyrimidines in liver mitochondria of mice deficient in NTH1 and OGG1 glycosylases J Biol Chem 278 2003 33701 33707 (Pubitemid 37553202)
61. R. Chattopadhyay, L. Wiederhold, B. Szczesny, I. Boldogh, T.K. Hazra, and T. Izumi Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells Nucleic Acids Res 34 2006 2067 2076 (Pubitemid 44314205)
62. B.B. Das, T.S. Dexheimer, K. Maddali, and Y. Pommier Role of tyrosyl-DNA phosphodiesterase (TDP1) in mitochondria Proc Natl Acad Sci USA 107 2010 19790 19795
63. P. Sykora, D.L. Croteau, V.A. Bohr, and D.M. Wilson 3rd. Aprataxin localizes to mitochondria and preserves mitochondrial function Proc Natl Acad Sci USA 108 2011 7437 7442
64. M.J. Longley, R. Prasad, D.K. Srivastava, S.H. Wilson, and W.C. Copeland Identification of 5′-deoxyribose phosphate lyase activity in human DNA polymerase gamma and its role in mitochondrial base excision repair in vitro Proc Natl Acad Sci USA 95 1998 12244 12248
65. P. Liu, and B. Demple DNA repair in mammalian mitochondria: much more than we thought? Environ Mol Mutagen 51 2010 417 426
66. H. Dou, S. Mitra, and T.K. Hazra Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2 J Biol Chem 278 2003 49679 49684 (Pubitemid 37548799)
67. B. Kavli, O. Sundheim, M. Akbari, M. Otterlei, H. Nilsen, and F. Skorpen hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup J Biol Chem 277 2002 39926 39936 (Pubitemid 35190979)
68. T. Arai, V.P. Kelly, O. Minowa, T. Noda, and S. Nishimura The study using wild-type and Ogg1 knockout mice exposed to potassium bromate shows no tumor induction despite an extensive accumulation of 8-hydroxyguanine in kidney DNA Toxicology 221 2006 179 186
69. M.K. Chan, M.T. Ocampo-Hafalla, V. Vartanian, P. Jaruga, G. Kirkali, and K.L. Koenig Targeted deletion of the genes encoding NTH1 and NEIL1 DNA N-glycosylases reveals the existence of novel carcinogenic oxidative damage to DNA DNA Repair (Amst) 8 2009 786 794
70. M.T. Ocampo, W. Chaung, D.R. Marenstein, M.K. Chan, A. Altamirano, and A.K. Basu Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity Mol Cell Biol 22 2002 6111 6121 (Pubitemid 34857831)
71. M.T. Russo, G. De Luca, P. Degan, E. Parlanti, E. Dogliotti, and D.E. Barnes Accumulation of the oxidative base lesion 8-hydroxyguanine in DNA of tumor-prone mice defective in both the Myh and Ogg1 DNA glycosylases Cancer Res 64 2004 4411 4414 (Pubitemid 38856910)
72. M. Takao, S. Kanno, K. Kobayashi, Q.M. Zhang, S. Yonei, and G.T. van der Horst A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue J Biol Chem 277 2002 42205 42213 (Pubitemid 35257539)
73. V. Vartanian, B. Lowell, I.G. Minko, T.G. Wood, J.D. Ceci, and S. George The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase Proc Natl Acad Sci USA 103 2006 1864 1869 (Pubitemid 43228784)
74. D. Banerjee, S.M. Mandal, A. Das, M.L. Hegde, S. Das, and K.K. Bhakat Preferential repair of oxidized base damage in the transcribed genes of mammalian cells J Biol Chem 286 2011 6006 6016
75. A. Das, I. Boldogh, J.W. Lee, J.A. Harrigan, M.L. Hegde, and J. Piotrowski The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1 J Biol Chem 282 2007 26591 26602 (Pubitemid 47443759)
76. H. Dou, C.A. Theriot, A. Das, M.L. Hegde, Y. Matsumoto, and I. Boldogh Interaction of the human DNA glycosylase NEIL1 with proliferating cell nuclear antigen. The potential for replication-associated repair of oxidized bases in mammalian genomes J Biol Chem 283 2008 3130 3140
77. M.L. Hegde, C.A. Theriot, A. Das, P.M. Hegde, Z. Guo, and R.K. Gary Physical and functional interaction between human oxidized base-specific DNA glycosylase NEIL1 and flap endonuclease 1 J Biol Chem 283 2008 27028 27037
78. C.A. Theriot, M.L. Hegde, T.K. Hazra, and S. Mitra RPA physically interacts with the human DNA glycosylase NEIL1 to regulate excision of oxidative DNA base damage in primer-template structures DNA Repair (Amst) 9 2010 643 652
79. S. Das, R. Chattopadhyay, K.K. Bhakat, I. Boldogh, K. Kohno, and R. Prasad Stimulation of NEIL2-mediated oxidized base excision repair via YB-1 interaction during oxidative stress J Biol Chem 282 2007 28474 28484 (Pubitemid 47606000)
80. R. Chattopadhyay, S. Das, A.K. Maiti, I. Boldogh, J. Xie, and T.K. Hazra Regulatory role of human AP-endonuclease (APE1/Ref-1) in YB-1-mediated activation of the multidrug resistance gene MDR1 Mol Cell Biol 28 2008 7066 7080
81. D.R. Marenstein, M.T. Ocampo, M.K. Chan, A. Altamirano, A.K. Basu, and R.J. Boorstein Stimulation of human endonuclease III by Y box-binding protein 1 (DNA-binding protein B). Interaction between a base excision repair enzyme and a transcription factor J Biol Chem 276 2001 21242 21249
82. Y. Liu, R. Prasad, and S.H. Wilson HMGB1: roles in base excision repair and related function Biochim Biophys Acta 1799 2010 119 130
83. J. Zhou, J. Ahn, S.H. Wilson, and C. Prives A role for p53 in base excision repair EMBO J 20 2001 914 923 (Pubitemid 32167655)
84. S.N. Kassam, and A.J. Rainbow UV-inducible base excision repair of oxidative damaged DNA in human cells Mutagenesis 24 2009 75 83
85. A.S. Jaiswal, L.B. Bloom, and S. Narayan Long-patch base excision repair of apurinic/apyrimidinic site DNA is decreased in mouse embryonic fibroblast cell lines treated with plumbagin: involvement of cyclin-dependent kinase inhibitor p21Waf-1/Cip-1 Oncogene 21 2002 5912 5922 (Pubitemid 35007242)
86. A.S. Jaiswal, S. Banerjee, H. Panda, C.D. Bulkin, T. Izumi, and F.H. Sarkar A novel inhibitor of DNA polymerase beta enhances the ability of temozolomide to impair the growth of colon cancer cells Mol Cancer 7 2009 1973 1983
87. S.H. Wilson, and T.A. Kunkel Passing the baton in base excision repair Nat Struct Biol 7 2000 176 178 (Pubitemid 30140755)
88. C.D. Mol, T. Izumi, S. Mitra, and J.A. Tainer DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected] Nature 403 2000 451 456 (Pubitemid 30073097)
89. M. Otterlei, E. Warbrick, T.A. Nagelhus, T. Haug, G. Slupphaug, and M. Akbari Post-replicative base excision repair in replication foci EMBO J 18 1999 3834 3844 (Pubitemid 29308862)
90. M.L. Hegde, T.K. Hazra, and S. Mitra Functions of disordered regions in mammalian early base excision repair proteins Cell Mol Life Sci 67 2010 3573 3587
91. S. Ikeda, T. Biswas, R. Roy, T. Izumi, I. Boldogh, and A. Kurosky 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 1998 21585 21593 (Pubitemid 28405328)
92. X. Liu, and R. Roy Truncation of amino-terminal tail stimulates activity of human endonuclease III (hNTH1) J Mol Biol 321 2002 265 276
93. S. Doublie, V. Bandaru, J.P. Bond, and S.S. Wallace The crystal structure of human endonuclease VIII-like 1 (NEIL1) reveals a zincless finger motif required for glycosylase activity Proc Natl Acad Sci USA 101 2004 10284 10289 (Pubitemid 38924917)
94. A.L. Lu, X. Li, Y. Gu, P.M. Wright, and D.Y. Chang Repair of oxidative DNA damage: mechanisms and functions Cell Biochem Biophys 35 2001 141 170 (Pubitemid 33622685)
95. P.R. Romero, S. Zaidi, Y.Y. Fang, V.N. Uversky, P. Radivojac, and C.J. Oldfield Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms Proc Natl Acad Sci USA 103 2006 8390 8395 (Pubitemid 43838465)
96. K. Gunasekaran, C.J. Tsai, S. Kumar, D. Zanuy, and R. Nussinov Extended disordered proteins: targeting function with less scaffold Trends Biochem Sci 28 2003 81 85 (Pubitemid 36165136)
97. C. Haynes, C.J. Oldfield, F. Ji, N. Klitgord, M.E. Cusick, and P. Radivojac Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes PLoS Comput Biol 2 2006 e100
98. K. Shimizu, and H. Toh Interaction between intrinsically disordered proteins frequently occurs in a human protein-protein interaction network J Mol Biol 392 2009 1253 1265
99. A.K. Dunker, M.S. Cortese, P. Romero, L.M. Iakoucheva, and V.N. Uversky Flexible nets. The roles of intrinsic disorder in protein interaction networks FEBS J 272 2005 5129 5148 (Pubitemid 41503146)
100. H.J. Dyson, and P.E. Wright Intrinsically unstructured proteins and their functions Nat Rev Mol Cell Biol 6 2005 197 208 (Pubitemid 40314921)
101. T. Mittag, L.E. Kay, and J.D. Forman-Kay Protein dynamics and conformational disorder in molecular recognition J Mol Recognit 23 2010 105 116
102. C. Dingwall, and R.A. Laskey Nuclear targeting sequences - a consensus? Trends Biochem Sci 16 1991 478 481
103. P. Radivojac, L.M. Iakoucheva, C.J. Oldfield, Z. Obradovic, V.N. Uversky, and A.K. Dunker Intrinsic disorder and functional proteomics Biophys J 92 2007 1439 1456 (Pubitemid 46393458)
104. E.B. Jackson, C.A. Theriot, R. Chattopadhyay, S. Mitra, and T. Izumi Analysis of nuclear transport signals in the human apurinic/apyrimidinic endonuclease (APE1/Ref1) Nucleic Acids Res 33 2005 3303 3312 (Pubitemid 41194474)
105. S. Ikeda, T. Kohmoto, R. Tabata, and Y. Seki Differential intracellular localization of the human and mouse endonuclease III homologs and analysis of the sorting signals DNA Repair (Amst) 1 2002 847 854 (Pubitemid 35239882)
106. M. Otterlei, T. Haug, T.A. Nagelhus, G. Slupphaug, T. Lindmo, and H.E. Krokan Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively Nucleic Acids Res 26 1998 4611 4617 (Pubitemid 28466607)
107. O.G. Berg, R.B. Winter, and P.H. von Hippel Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory Biochemistry 20 1981 6929 6948
108. D. Vuzman, A. Azia, and Y. Levy Searching DNA via a "Monkey Bar" mechanism: the significance of disordered tails J Mol Biol 396 2010 674 684
109. D. Vuzman, and Y. Levy DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail Proc Natl Acad Sci USA 107 2010 21004 21009
110. D. Vuzman, M. Polonsky, and Y. Levy Facilitated DNA search by multidomain transcription factors: cross talk via a flexible linker Biophys J 99 2010 1202 1211
111. A. Toth-Petroczy, I. Simon, M. Fuxreiter, and Y. Levy Disordered tails of homeodomains facilitate DNA recognition by providing a trade-off between folding and specific binding J Am Chem Soc 131 2009 15084 15085
112. J. Iwahara, M. Zweckstetter, and G.M. Clore NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA Proc Natl Acad Sci USA 103 2006 15062 15067 (Pubitemid 44583164)
113. A.R. Dunn, N.M. Kad, S.R. Nelson, D.M. Warshaw, and S.S. Wallace Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA Nucleic Acids Res 17 2011 7487 7498
114. K.E. Krueger, and S. Srivastava Posttranslational protein modifications: current implications for cancer detection, prevention, and therapeutics Mol Cell Proteomics 5 2006 1799 1810 (Pubitemid 44688189)
115. B.T. Seet, I. Dikic, M.M. Zhou, and T. Pawson Reading protein modifications with interaction domains Nat Rev Mol Cell Biol 7 2006 473 483 (Pubitemid 44036453)
116. K.K. Bhakat, T. Izumi, S.H. Yang, T.K. Hazra, and S. Mitra Role of acetylated human AP-endonuclease (APE1/Ref-1) in regulation of the parathyroid hormone gene EMBO J 22 2003 6299 6309 (Pubitemid 37522587)
117. C.S. Busso, T. Iwakuma, and T. Izumi Ubiquitination of mammalian AP endonuclease (APE1) regulated by the p53-MDM2 signaling pathway Oncogene 28 2009 1616 1625
118. H. Lee, K.H. Mok, R. Muhandiram, K.H. Park, J.E. Suk, and D.H. Kim Local structural elements in the mostly unstructured transcriptional activation domain of human p53 J Biol Chem 275 2000 29426 29432 (Pubitemid 32043817)
119. D. Fantini, C. Vascotto, D. Marasco, C. D'Ambrosio, M. Romanello, and L. Vitagliano Critical lysine residues within the overlooked N-terminal domain of human APE1 regulate its biological functions Nucleic Acids Res 38 2010 8239 8256
120. A. Bhattacharyya, R. Chattopadhyay, B.R. Burnette, J.V. Cross, S. Mitra, and P.B. Ernst Acetylation of apurinic/apyrimidinic endonuclease-1 regulates Helicobacter pylori-mediated gastric epithelial cell apoptosis Gastroenterology 136 2009 2258 2269
121. S. Sengupta, A.K. Mantha, S. Mitra, and K.K. Bhakat Human AP endonuclease (APE1/Ref-1) and its acetylation regulate YB-1-p300 recruitment and RNA polymerase II loading in the drug-induced activation of multidrug resistance gene MDR1 Oncogene 30 2010 482 493
122. K.K. Bhakat, T.K. Hazra, and S. Mitra Acetylation of the human DNA glycosylase NEIL2 and inhibition of its activity Nucleic Acids Res 32 2004 3033 3039 (Pubitemid 39022994)
123. M. Tini, A. Benecke, S.J. Um, J. Torchia, R.M. Evans, and P. Chambon Association of CBP/p300 acetylase and thymine DNA glycosylase links DNA repair and transcription Mol Cell 9 2002 265 277 (Pubitemid 34195553)
124. K.K. Bhakat, S.K. Mokkapati, I. Boldogh, T.K. Hazra, and S. Mitra Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo Mol Cell Biol 26 2006 1654 1665
125. M.M. Hsieh, V. Hegde, M.R. Kelley, and W.A. Deutsch Activation of APE/Ref-1 redox activity is mediated by reactive oxygen species and PKC phosphorylation Nucleic Acids Res 29 2001 3116 3122 (Pubitemid 32685238)
126. A. Yacoub, M.R. Kelley, and W.A. Deutsch The DNA repair activity of human redox/repair protein APE/Ref-1 is inactivated by phosphorylation Cancer Res 57 1997 5457 5459 (Pubitemid 28006746)
127. K.K. Bhakat, A.K. Mantha, and S. Mitra Transcriptional regulatory functions of mammalian AP-endonuclease (APE1/Ref-1), an essential multifunctional protein Antioxid Redox Signal 11 2009 621 638
128. G. Fritz, and B. Kaina Phosphorylation of the DNA repair protein APE/REF-1 by CKII affects redox regulation of AP-1 Oncogene 18 1999 1033 1040 (Pubitemid 29086280)
129. J.L. Parsons, I.I. Dianova, D. Finch, P.S. Tait, C.E. Strom, and T. Helleday XRCC1 phosphorylation by CK2 is required for its stability and efficient DNA repair DNA Repair (Amst) 9 2010 835 841
130. E. Huang, D. Qu, Y. Zhang, K. Venderova, M.E. Haque, and M.W. Rousseaux The role of Cdk5-mediated apurinic/apyrimidinic endonuclease 1 phosphorylation in neuronal death Nat Cell Biol 12 2010 563 571
131. X. Lu, D. Bocangel, B. Nannenga, H. Yamaguchi, E. Appella, and L.A. Donehower The p53-induced oncogenic phosphatase PPM1D interacts with uracil DNA glycosylase and suppresses base excision repair Mol Cell 15 2004 621 634 (Pubitemid 39141788)
132. L. Hagen, B. Kavli, M.M. Sousa, K. Torseth, N.B. Liabakk, and O. Sundheim Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA EMBO J 27 2008 51 61
133. Y. Gu, and A.L. Lu Differential DNA recognition and glycosylase activity of the native human MutY homolog (hMYH) and recombinant hMYH expressed in bacteria Nucleic Acids Res 29 2001 2666 2674 (Pubitemid 32600325)
134. F. Dantzer, L. Luna, M. Bjoras, and E. Seeberg Human OGG1 undergoes serine phosphorylation and associates with the nuclear matrix and mitotic chromatin in vivo Nucleic Acids Res 30 2002 2349 2357 (Pubitemid 34618985)
135. J.L. Parsons, P.S. Tait, D. Finch, I.I. Dianova, M.J. Edelmann, and S.V. Khoronenkova Ubiquitin ligase ARF-BP1/Mule modulates base excision repair EMBO J 28 2009 3207 3215
136. V. Chau, J.W. Tobias, A. Bachmair, D. Marriott, D.J. Ecker, and D.K. Gonda A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein Science 243 1989 1576 1583 (Pubitemid 19090506)
137. C.S. Busso, M.W. Lake, and T. Izumi Posttranslational modification of mammalian AP endonuclease (APE1) Cell Mol Life Sci 67 2010 3609 3620
138. S.M. Nijman, M.P. Luna-Vargas, A. Velds, T.R. Brummelkamp, A.M. Dirac, and T.K. Sixma A genomic and functional inventory of deubiquitinating enzymes Cell 123 2005 773 786 (Pubitemid 41721026)
139. C.S. Busso, C.M. Wedgeworth, and T. Izumi Ubiquitination of human AP-endonuclease 1 (APE1) enhanced by T233E substitution and by CDK5 Nucleic Acids Res 39 2011 8017 8028
140. J.A. Fischer, S. Muller-Weeks, and S. Caradonna Proteolytic degradation of the nuclear isoform of uracil-DNA glycosylase occurs during the S phase of the cell cycle DNA Repair (Amst) 3 2004 505 513 (Pubitemid 38482025)
141. J. Chen, W. Bozza, and Z. Zhuang Ubiquitination of PCNA and its essential role in eukaryotic translesion synthesis Cell Biochem Biophys 60 2011 47 60
142. A.R. Lehmann Ubiquitin-family modifications in the replication of DNA damage FEBS Lett 585 2011 2772 2779
143. S. Katyal, and P.J. McKinnon DNA strand breaks, neurodegeneration and aging in the brain Mech Ageing Dev 129 2008 483 491
144. N. Al-Tassan, N.H. Chmiel, J. Maynard, N. Fleming, A.L. Livingston, and G.T. Williams Inherited variants of MYH associated with somatic G:C→T:A mutations in colorectal tumors Nat Genet 30 2002 227 232
145. M. Goodenberger, and N.M. Lindor Lynch syndrome and MYH-associated polyposis: review and testing strategy J Clin Gastroenterol 45 2011 488 500
146. S. Boiteux, and J.P. Radicella The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis Arch Biochem Biophys 377 2000 1 8 (Pubitemid 30257280)
147. K. Shinmura, and J. Yokota The OGG1 gene encodes a repair enzyme for oxidatively damaged DNA and is involved in human carcinogenesis Antioxid Redox Signal 3 2001 597 609 (Pubitemid 32785983)
148. C. Dherin, J.P. Radicella, M. Dizdaroglu, and S. Boiteux Excision of oxidatively damaged DNA bases by the human alpha-hOgg1 protein and the polymorphic alpha-hOgg1(Ser326Cys) protein which is frequently found in human populations Nucleic Acids Res 27 1999 4001 4007 (Pubitemid 29479026)
149. J.W. Hill, and M.K. Evans Dimerization and opposite base-dependent catalytic impairment of polymorphic S326C OGG1 glycosylase Nucleic Acids Res 34 2006 1620 1632
150. J.M. Weiss, E.L. Goode, W.C. Ladiges, and C.M. Ulrich Polymorphic variation in hOGG1 and risk of cancer: a review of the functional and epidemiologic literature Mol Carcinog 42 2005 127 141 (Pubitemid 40271142)
151. A. Klungland, I. Rosewell, S. Hollenbach, E. Larsen, G. Daly, and B. Epe Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage Proc Natl Acad Sci USA 96 1999 13300 13305
152. M. Osterod, S. Hollenbach, J.G. Hengstler, D.E. Barnes, T. Lindahl, and B. Epe Age-related and tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1) deficient mice Carcinogenesis 22 2001 1459 1463 (Pubitemid 32898703)
153. Y. Xie, H. Yang, C. Cunanan, K. Okamoto, D. Shibata, and J. Pan Deficiencies in mouse Myh and Ogg1 result in tumor predisposition and G to T
154. J.L. Parsons, and R.H. Elder DNA N-glycosylase deficient mice: a tale of redundancy Mutat Res 531 2003 165 175 (Pubitemid 37456730)
155. D.M. Wilson 3rd, and V.A. Bohr The mechanics of base excision repair, and its relationship to aging and disease DNA Repair (Amst) 6 2007 544 559 (Pubitemid 46357056)
156. E.C. Friedberg, G.C. Walker, W. Siede, R.D. Wood, R.A. Schultz, and T. Ellenberger DNA repair and mutagenesis 2nd ed. 2006 ASM Press Washington
157. D.M. Wilson 3rd, and L.H. Thompson Life without DNA repair Proc Natl Acad Sci USA 94 1997 12754 12757 (Pubitemid 27518420)
158. L. Zheng, H. Dai, M.L. Hegde, M. Zhou, Z. Guo, and X. Wu Fen1 mutations that specifically disrupt its interaction with PCNA cause aneuploidy-associated cancer Cell Res 21 2011 1052 1067
159. L. Zheng, H. Dai, M. Zhou, M. Li, P. Singh, and J. Qiu Fen1 mutations result in autoimmunity, chronic inflammation and cancers Nat Med 13 2007 812 819 (Pubitemid 47038189)
160. D. Starcevic, S. Dalal, and J.B. Sweasy Is there a link between DNA polymerase beta and cancer? Cell Cycle 3 2004 998 1001 (Pubitemid 40268650)
161. T. Lang, M. Maitra, D. Starcevic, S.X. Li, and J.B. Sweasy A DNA polymerase beta mutant from colon cancer cells induces mutations Proc Natl Acad Sci USA 101 2004 6074 6079 (Pubitemid 38520530)
162. J.J. Hu, T.R. Smith, M.S. Miller, H.W. Mohrenweiser, A. Golden, and L.D. Case Amino acid substitution variants of APE1 and XRCC1 genes associated with ionizing radiation sensitivity Carcinogenesis 22 2001 917 922 (Pubitemid 32514958)
163. L. Jiao, M.L. Bondy, M.M. Hassan, R.A. Wolff, D.B. Evans, and J.L. Abbruzzese Selected polymorphisms of DNA repair genes and risk of pancreatic cancer Cancer Detect Prev 30 2006 284 291 (Pubitemid 44163055)
164. E.L. Goode, C.M. Ulrich, and J.D. Potter Polymorphisms in DNA repair genes and associations with cancer risk Cancer Epidemiol Biomarkers Prev 11 2002 1513 1530 (Pubitemid 36020002)
165. R.J. Hung, J. Hall, P. Brennan, and P. Boffetta Genetic polymorphisms in the base excision repair pathway and cancer risk: a HuGE review Am J Epidemiol 162 2005 925 942 (Pubitemid 41619464)
166. P.C. Hanawalt Emerging links between premature ageing and defective DNA repair Mech Ageing Dev 129 2008 503 505
167. M. Obulesu, and D.M. Rao DNA damage and impairment of DNA repair in Alzheimer's disease Int J Neurosci 120 2010 397 403
168. K. Subba Rao Mechanisms of disease: DNA repair defects and neurological disease Nat Clin Pract Neurol 3 2007 162 172
169. L. Weissman, D.G. Jo, M.M. Sorensen, N.C. de Souza-Pinto, W.R. Markesbery, and M.P. Mattson Defective DNA base excision repair in brain from individuals with Alzheimer's disease and amnestic mild cognitive impairment Nucleic Acids Res 35 2007 5545 5555 (Pubitemid 47423927)
170. S. Dogru-Abbasoglu, G. Aykac-Toker, H.A. Hanagasi, H. Gurvit, M. Emre, and M. Uysal The Arg194Trp polymorphism in DNA repair gene XRCC1 and the risk for sporadic late-onset Alzheimer's disease Neurol Sci 28 2007 31 34 (Pubitemid 46502077)
171. L. Migliore, I. Fontana, F. Trippi, R. Colognato, F. Coppede, and G. Tognoni Oxidative DNA damage in peripheral leukocytes of mild cognitive impairment and AD patients Neurobiol Aging 26 2005 567 573 (Pubitemid 40228745)
172. S. Milutinovic, Q. Zhuang, and M. Szyf Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification J Biol Chem 277 2002 20974 20978 (Pubitemid 34967408)
173. S.F. el-Khamisy, and K.W. Caldecott DNA single-strand break repair and spinocerebellar ataxia with axonal neuropathy-1 Neuroscience 145 2007 1260 1266 (Pubitemid 46602725)
174. J. Shen, E.C. Gilmore, C.A. Marshall, M. Haddadin, J.J. Reynolds, and W. Eyaid Mutations in PNKP cause microcephaly, seizures and defects in DNA repair Nat Genet 42 2010 245 249
175. F. Coppede, R. Ceravolo, F. Migheli, F. Fanucchi, D. Frosini, and G. Siciliano The hOGG1 Ser326Cys polymorphism is not associated with sporadic Parkinson's disease Neurosci Lett 473 2010 248 251
176. F. Coppede, M. Mancuso, A. Lo Gerfo, C. Carlesi, S. Piazza, and A. Rocchi Association of the hOGG1 Ser326Cys polymorphism with sporadic amyotrophic lateral sclerosis Neurosci Lett 420 2007 163 168 (Pubitemid 46824158)
177. F. Coppede, M. Mancuso, A. Lo Gerfo, M.L. Manca, L. Petrozzi, and L. Migliore A Ser326Cys polymorphism in the DNA repair gene hOGG1 is not associated with sporadic Alzheimer's disease Neurosci Lett 414 2007 282 285
178. F. Coppede, and L. Migliore DNA damage and repair in Alzheimer's disease Curr Alzheimer Res 6 2009 36 47
179. C. Hayward, S. Colville, R.J. Swingler, and D.J. Brock Molecular genetic analysis of the APEX nuclease gene in amyotrophic lateral sclerosis Neurology 52 1999 1899 1901 (Pubitemid 29260908)
180. R. Hirano, H. Interthal, C. Huang, T. Nakamura, K. Deguchi, and K. Choi Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation? EMBO J 26 2007 4732 4743 (Pubitemid 350126790)
181. U. Rass, I. Ahel, and S.C. West Actions of aprataxin in multiple DNA repair pathways J Biol Chem 282 2007 9469 9474 (Pubitemid 47104565)
182. M.L. Hegde, P.M. Hegde, L.M. Holthauzen, T.K. Hazra, K.S. Rao, and S. Mitra Specific Inhibition of NEIL-initiated repair of oxidized base damage in human genome by copper and iron: potential etiological linkage to neurodegenerative diseases J Biol Chem 285 2010 28812 28825
183. M.L. Hegde, P.M. Hegde, K.S. Jagannatha Rao, and S. Mitra Oxidative genome damage and its repair in neurodegenerative diseases: function of transition metals as a double-edged sword J Alzheimers Dis 24 2011 183 198
184. J.R. Whiteside, C.L. Box, T.J. McMillan, and S.L. Allinson Cadmium and copper inhibit both DNA repair activities of polynucleotide kinase DNA Repair (Amst) 9 2010 83 89
185. H. Li, R. Swiercz, and E.W. Englander Elevated metals compromise repair of oxidative DNA damage via the base excision repair pathway: implications of pathologic iron overload in the brain on integrity of neuronal DNA J Neurochem 110 2009 1774 1783
186. M.S. Bobola, A. Blank, M.S. Berger, B.A. Stevens, and J.R. Silber Apurinic/apyrimidinic endonuclease activity is elevated in human adult gliomas Clin Cancer Res 7 2001 3510 3518 (Pubitemid 33069988)
187. M.S. Bobola, M.J. Emond, A. Blank, E.H. Meade, D.D. Kolstoe, and M.S. Berger Apurinic endonuclease activity in adult gliomas and time to tumor progression after alkylating agent-based chemotherapy and after radiotherapy Clin Cancer Res 10 2004 7875 7883 (Pubitemid 39587526)
188. M.S. Bobola, L.S. Finn, R.G. Ellenbogen, J.R. Geyer, M.S. Berger, and J.M. Braga Apurinic/apyrimidinic endonuclease activity is associated with response to radiation and chemotherapy in medulloblastoma and primitive neuroectodermal tumors Clin Cancer Res 11 2005 7405 7414 (Pubitemid 41507701)
189. D.M. Wilson 3rd, and A. Simeonov Small molecule inhibitors of DNA repair nuclease activities of APE1 Cell Mol Life Sci 67 2010 3621 3631
190. M.L. Fishel, Y. Jiang, N.V. Rajeshkumar, G. Scandura, A.L. Sinn, and Y. He Impact of APE1/Ref-1 redox inhibition on pancreatic tumor growth Mol Cancer Ther 10 2011 1698 1708
191. A. Bapat, L.S. Glass, M. Luo, M.L. Fishel, E.C. Long, and M.M. Georgiadis Novel small-molecule inhibitor of apurinic/apyrimidinic endonuclease 1 blocks proliferation and reduces viability of glioblastoma cells J Pharmacol Exp Ther 334 2010 988 998
192. A. Ashworth A synthetic lethal therapeutic approach: poly(ADP) ribose polymerase inhibitors for the treatment of cancers deficient in DNA double-strand break repair J Clin Oncol 26 2008 3785 3790
193. H. Farmer, N. McCabe, C.J. Lord, A.N. Tutt, D.A. Johnson, and T.B. Richardson Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy Nature 434 2005 917 921 (Pubitemid 40559006)
194. D.A. Loser, A. Shibata, A.K. Shibata, L.J. Woodbine, P.A. Jeggo, and A.J. Chalmers Sensitization to radiation and alkylating agents by inhibitors of poly(ADP-ribose) polymerase is enhanced in cells deficient in DNA double-strand break repair Mol Cancer Ther 9 2010 1775 1787
195. F.V. Rassool, and A.E. Tomkinson Targeting abnormal DNA double strand break repair in cancer Cell Mol Life Sci 67 2010 3699 3710