Structural Features of DNA Glycosylases and AP Endonucleases

DNA Damage Recognition

Volumn , Issue , 2005, Pages 299-322

  Huffman, Joy L ^a   Sundheim, Ottar ^a   Tainer, John A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 47849121026     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9780849352683-20     Document Type: Chapter

References (113)

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993; 362:709-715.
2. Das SK. Harmful health effects of cigarette smoking. Mol Cell Biochem 2003; 253: 159-165.
3. Ames BN, Gold LS, Willett WC. The causes and prevention of cancer. Proc Natl Acad Sci USA 1995; 92:5258-5265.
4. Memisoglu A, Samson L. Base excision repair in yeast and mammals. Mutat Res 2000; 451:39-51.
5. Dogliotti E, Fortini P, Pascucci B, Parlanti E. The mechanism of switching among multiple BER pathways. Prog Nucleic Acid Res Mol Biol 2001; 68:3-27.
6. Seeberg E, Eide L, Bjoras M. The base excision repair pathway. Trends Biochem Sci 1995; 20:391-397.
7. Dodson ML, Michaels ML, Lloyd RS. Unified catalytic mechanism for DNA glycosy-lases. J Biol Chem 1994; 269:32709-32712.
8. Tchou J, Grollman AP. The catalytic mechanism of Fpg protein. Evidence for a Schiff base intermediate and amino terminus localization of the catalytic site. J Biol Chem 1995; 270:11671-11677.
9. Fromme JC, Verdine GL. Structural insights into lesion recognition and repair by the bacterial 8-oxoguanine DNA glycosylase MutM. Nat Struct Biol 2002; 9:544-552.
10. Fromme JC, Verdine GL. Structure of a trapped endonuclease III-DNA covalent intermediate. EMBO J 2003; 22:3461-3471.
11. Fromme JC, Bruner SD, Yang W, Karplus M, Verdine GL. Product-assisted catalysis in base-excision DNA repair. Nat Struct Biol 2003; 10:204-211.
12. Gilboa R, Zharkov DO, Golan G, Fernandes AS, Gerchman SE, Matz E, Kycia JH, Grollman AP, Shoham G. Structure of formamidopyrimidine-DNA glycosylase covalently complexed to DNA. J Biol Chem 2002; 277:19811-19816.
13. Zharkov DO, Golan G, Gilboa R, Fernandes AS, Gerchman SE, Kycia JH, Rieger RA, Grollman AP, Shoham G. Structural analysis of an Escherichia coli endonuclease VIII covalent reaction intermediate. EMBO J 2002; 21:789-800.
14. Williams SD, David SS. Evidence that MutY is a monofunctional glycosylase capable of forming a covalent Schiff base intermediate with substrate DNA. Nucleic Acids Res 1998; 26:5123-5133.
15. Thayer MM, Ahern H, Xing D, Cunningham RP, Tainer JA. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J 1995; 14:4108-4120.
16. Yamagata Y, Kato M, Odawara K, Tokuno Y, Nakashima Y, Matsushima N, Yasumura K, Tomita K, Ihara K, Fujii Y, Nakabeppu Y, Sekiguchi M, Fujii S. Three-dimensional structure of a DNA repair enzyme, 3-methyladenine DNA glycosy-lase II, from Escherichia coli. Cell 1996; 86:311-319.
17. Kuo CF, McRee DE, Fisher CL, O’Handley SF, Cunningham RP, Tainer JA. Atomic strucute of the DNA repair [4Fe-4S] enzyme endonuclease III. Science 1992; 258: 434-440.
18. Bruner SD, Norman DP, Verdine GL. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 2000; 403:859-866.
19. Eichman BF, O’Rourke EJ, Radicella JP, Ellenberger T. Crystal structures of 3-mehtyladenine DNA glycoslyase MagIII and the recognition of alkylated bases. EMBO J 2003; 22:4898-4909.
20. Vassylyev DG, Kashiwagi T, Mikami Y, Ariyoshi M, Iwai S, Ohtsuka E, Morikawa K. Atomic model of a pyrimidine dimer excision repair enzyme complexed with a DNA substrate: structural basis for damaged DNA recognition. Cell 1995; 83:773-782.
21. Mol CD, Arvai AS, Begley TJ, Cunningham RP, Tainer JA. Structure and activity of a thermostable thymine-DNA glycosylase: evidence for base twisting to remove mismatched normal DNA bases. J Mol Biol 2002; 315:373-384.
22. Labahn J, Scharer OD, Long A, Ezaz-Nikpay K, Verdine GL, Ellenberger TE. Structural basis for the excision repair of alkylation-damaged DNA. Cell 1996; 86:321-329.
23. Guan Y, Manuel RC, Arvai AS, Parikh SS, Mol CD, Miller JH, Lloyd S, Tainer JA. MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat Struct Biol 1998; 5:1058-1064.
24. Drohat AC, Kwon K, Krosky DJ, Stivers JT. 3-Methyladenine DNA glycosylase I is an unexpected helix-hairpin-helix superfamily member. Nat Struct Biol 2002; 9:659-664.
25. Hollis T, Ichikawa Y, Ellenberger T. DNA bending and a flip-out mechanism for base excision by the helix-hairpin-helix DNA glycosylase, Escherichia coli AlkA. EMBO J 2000; 19:758-766.
26. Lau AY, Scharer OD, Samson L, Verdine GL, Ellenberger T. Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell 1998; 95:249-258.
27. Doherty AJ, Serpell LC, Ponting CP. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res 1996; 24:2488-2497.
28. Hosfield DJ, Mol CD, Shen B, Tainer JA. Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: coupling DNA and PCNA binding to FEN-1 activity. Cell 1998; 95:135-146.
29. Sugahara M, Mikawa T, Kumasaka T, Yamamoto M, Kato R, Fukuyama K, Inoue Y, Kuramitsu S. Crystal strucure of a repair enzyme of oxidatively damaged DNA, MutM (Fpg), from an extreme thermophile, Thermus thermophilus HB8. EMBO J 2000; 19: 3857-3869.
30. Serre L, Pereira de Jesus K, Boiteux S, Zelwer C, Castaing B. Crystal structure of the Lactococcus lactis formamidopyrimidine-DNA glycosylase bound to an abasic site analouge-containing DNA. EMBO J 2002; 21:2854-2865.
31. Fromme JC, Verdine GL. DNA lesion recognition by the bacterial repair enzyme MutM. J Biol Chem 2003.
32. Hazra TK, Izumi T, Boldogh I, Imhoff B, Kow YW, Jaruga P, Dizdaroglu M, Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc Natl Acad Sci USA 2002; 99:3523-3528.
33. Hazra TK, Izumi T, Venkataraman R, Kow YW, Dizdaroglu M, Mitra S. Characterization of a novel 8-oxoguanine-DNA glycosylase activity in Escherichia coli and identification of the enzyme as endonuclease VIII. J Biol Chem 2000; 275:27762-27767.
34. Takao M, Kanno SI, Kobayashi K, Zhang QM, Yonei S, Van Der Horst GT, Yasui A. A Back-up Glycosylase in Nth1 Knock-out Mice Is a Functional Nei (Endonuclease VIII) Homologue. J Biol Chem 2002; 277:42205-42213.
35. Radicella JP, Dherin C, Desmaze C, Fox MS, Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 1997; 94:8010-8015.
36. Ikeda S, Biswas T, Roy R, Izumi T, Boldogh I, Kurosky A, Sarker AH, Seki S, Mitra S. Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue. J Biol Chem 1998; 273:21585-21593.
37. Hazra TK, Kow YW, Hatahet Z, Imhoff B, Boldogh I, Mokkapati SK, Mitra S, Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J Biol Chem 2002; 277:30417-30420.
38. Bjoras M, Luna L, Johnsen B, Hoff E, Haug T, Rognes T, Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7, 8-dihydro-8-oxoguanine and abasic sites. EMBO J 1997; 16:6314-6322.
39. Bjoras M, Seeberg E, Luna L, Pearl LH, Barrett TE. Reciprocal ‘‘flipping’’ underlies substrate recognition and catalytic activation by the human 8-oxo-guanine DNA glyco-sylase. J Mol Biol 2002; 317:171-177.
40. Zharkov DO, Gilboa R, Yagil I, Kycia JH, Gerchman SE, Shoham G, Grollman AP. Role for lysine 142 in the excision of adenine from A:G mispairs by MutY DNA glycosylase of Escherichia coli. Biochemistry 2000; 39:14768-14778.
41. Michaels ML, Miller JH. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J Bacteriol 1992; 174:6321-6325.
42. Abeygunawardana C, Weber DJ, Gittis AG, Frick DN, Lin J, Miller AF, Bessman MJ, Mildvan AS. Solution structure of the MutT enzyme, a nucleoside triphosphate pyro-phosphohydrolase. Biochemistry 1995; 34:14997-15005.
43. Noll DM, Gogos A, Granek JA, Clarke ND. The C-terminal domain of the adenine-DNA glycosylase MutY confers specificity for 8-oxoguanine adenine mispairs and may have evolved from MutT, an 8-oxo-dGTPase. Biochemistry 1999; 38:6374-6379.
44. Volk DE, House PG, Thiviyanathan V, Luxon BA, Zhang S, Lloyd RS, Gorenstein DG. Structural similarities between MutT and the C-terminal domain of MutY. Biochemistry 2000; 39:7331-7336.
45. Bernards AS, Miller JK, Bao KK, Wong I. Flipping duplex DNA inside out: a double base-flipping reaction mechanism by Escherichia coli MutY adenine glycosylase. J Biol Chem 2002; 277:20960-20964.
46. Wist E, Unhjem O, Krokan H. Accumulation of small fragments of DNA in isolated HeLa cell nuclei due to transient incorporation of dUMP. Biochim Biophys Acta 1978; 520:253-270.
47. Tye BK, Nyman PO, Lehman IR, Hochhauser S, Weiss B. Transient accumulation of Okazaki fragments as a result of uracil incorporation into nascent DNA. Proc Natl Acad Sci USA 1977; 74:154-157.
48. Nilsen H, Otterlei M, Haug T, Solum K, Nagelhus TA, Skorpen F, Krokan HE. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Res 1997; 25:750-755.
49. Savva R, McAuley-Hecht K, Brown T, Pearl L. The structural basis of specific base-excision repair by uracil-DNA glycosylase. Nature 1995; 373:487-493.
50. Slupphaug G, Mol CD, Kavli B, Arvai AS, Krokan HE, Tainer JA. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 1996; 384:87-92.
51. Xiao G, Tordova M, Jagadeesh J, Drohat AC, Stivers JT, Gilliland GL. Crystal structure of Escherichia coli uracil DNA glycosylase and its complexes with uracil and glycerol: structure and glycosylase mechanism revisited. Proteins 1999; 35:13-24.
52. Leiros I, Moe E, Lanes O, Smalas AO, Willassen NP. The structure of uracil-DNA glycosylase from Atlantic cod (Gadus morhua) reveals cold-adaptation features. Acta Crystallogr D Biol Crystallogr 2003; 59:1357-1365.
53. Parikh SS, Mol CD, Slupphaug G, Bharati S, Krokan HE, Tainer JA. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J 1998; 17:5214-5226.
54. Wong I, Lundquist AJ, Bernards AS, Mosbaugh DW. Presteady-state analysis of a single catalytic turnover by Escherichia coli uracil-DNA glycosylase reveals a ‘‘pinch-pull-push’’ mechanism. J Biol Chem 2002; 277:19424-19432.
55. Pearl LH. Structure and function in the uracil-DNA glycosylase superfamily. Mutat Res 2000; 460:165-181.
56. Brown TC, Jiricny J. A specific mismatch repair event protects mammalian cells from loss of 5-methylcytosine. Cell 1987; 50:945-950.
57. Hardeland U, Bentele M, Lettieri T, Steinacher R, Jiricny J, Schar P. Thymine DNA glycosylase. Prog Nucleic Acid Res Mol Biol 2001; 68:235-253.
58. Gallinari P, Jiricny J. A new class of uracil-DNA glycosylases related to human thymine-DNA glycosylase. Nature 1996; 383:735-738.
59. Hang B, Medina M, Fraenkel-Conrat H, Singer B. A 55-kDa protein isolated from human cells shows DNA glycosylase activity toward 3, N4-ethenocytosine and the G/T mismatch. Proc Natl Acad Sci USA 1998; 95:13561-13566.
60. Barrett TE, Savva R, Panayotou G, Barlow T, Brown T, Jiricny J, Pearl LH. Crystal structure of a G:T/U mismatch-specific DNA glycosylase: mismatch recognition by complementary-strand interactions. Cell 1998; 92:117-129.
61. Barrett TE, Scharer OD, Savva R, Brown T, Jiricny J, Verdine GL, Pearl LH. Crystal structure of a thwarted mismatch glycosylase DNA repair complex. EMBO J 1999; 18:6599-6609.
62. Haushalter KA, Todd Stukenberg MW, Kirschner MW, Verdine GL. Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors. Curr Biol 1999; 9:174-185.
63. Kavli B, Sundheim O, Akbari M, Otterlei M, Nilsen H, Skorpen F, Aas PA, Hagen L, Krokan HE, Slupphaug G. 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 2002; 277:39926-39936.
64. Boorstein RJ, Cummings A Jr., Marenstein DR, Chan MK, Ma Y, Neubert TA, Brown SM, Teebor GW. Definitive identification of mammalian 5-hydroxymethyluracil DNA N-glycosylase activity as SMUG1. J Biol Chem 2001; 276:41991-41997.
65. Wibley JE, Waters TR, Haushalter K, Verdine GL, Pearl LH. Structure and specificity of the vertebrate anti-mutator uracil-DNA glycosylase SMUG1. Mol Cell 2003; 11: 1647-1659.
66. Hoseki J, Okamoto A, Masui R, Shibata T, Inoue Y, Yokoyama S, Kuramitsu S. Crystal structure of a family 4 uracil-DNA glycosylase from Thermus thermophilus HB8. J Mol Biol 2003; 333:515-526.
67. Petronzelli F, Riccio A, Markham GD, Seeholzer SH, Genuardi M, Karbowski M, Yeung AT, Matsumoto Y, Bellacosa A. Investigation of the substrate spectrum of the human mismatch-specific DNA N-glycosylase MED1 (MBD4): fundamental role of the catalytic domain. J Cell Physiol 2000; 185:473-480.
68. Parikh SS, Walcher G, Jones GD, Slupphaug G, Krokan HE, Blackburn GM, Tainer JA. Uracil-DNA glycosylase-DNA substrate and product structures: conformational strain promotes catalytic efficiency by coupled stereoelectronic effects. Proc Natl Acad Sci USA 2000; 97:5083-5088.
69. Ohki I, Shimotake N, Fujita N, Nakao M, Shirakawa M. Solution structure of the methyl-CpG-binding domain of the methylation-dependent transcriptional repressor MBD1. EMBO J 1999; 18:6653-6661.
70. Ohki I, Shimotake N, Fujita N, Jee J, Ikegami T, Nakao M, Shirakawa M. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 2001; 105:487-497.
71. Wakefield RI, Smith BO, Nan X, Free A, Soteriou A, Uhrin D, Bird AP, Barlow PN. The solution structure of the domain from MeCP2 that binds to methylated DNA. J Mol Biol 1999; 291:1055-1065.
72. Wu P, Qiu C, Sohail A, Zhang X, Bhagwat AS, Cheng X. Mismatch repair in methylated DNA. Structure and activity of the mismatch-specific thymine glycosylase domain of methyl-CpG-binding protein MBD4. J Biol Chem 2003; 278:5285-5291.
73. Huffman JL, Li H, White RH, Tainer JA. Structural basis for recognition and catalysis by the bifunctional dCTP deaminase and dUTPase from Methanococcus jannaschii. J Mol Biol 2003; 331:885-896.
74. Mol CD, Harris JM, McIntosh EM, Tainer JA. Human dUTP pyrophosphatase: uracil recognition by a beta hairpin and active sites formed by three separate subunits. Structure 1996; 4:1077-1092.
75. Bjornberg O, Neuhard J, Nyman PO. A bifunctional dCTP deaminase-dUTP nucleoti-dohydrolase from the hyperthermophilic archeon Methanococcus jannaschii. J Biol Chem 2003.
76. Dauter Z, Persson R, Rosengren AM, Nyman PO, Wilson KS, Cedergren-Zeppezauer ES. Crystal structure of dUTPase from equine infectious anaemia virus; active site metal binding in a substrate analogue complex. J Mol Biol 1999; 285:655-673.
77. Cedergren-Zeppezauer ES, Larsson G, Nyman PO, Dauter Z, Wilson KS. Crystal structure of a dUTPase. Nature 1992; 355:740-743.
78. Prasad GS, Stura EA, McRee DE, Laco GS, Hasselkus-Light C, Elder JH, Stout CD. Crystal structure of dUTP pyrophosphatase from feline immunodeficiency virus. Protein Sci 1996; 5:2429-2437.
79. Daniels DS, Mol CD, Arvai AS, Kanugula S, Pegg AE, Tainer JA. Active and alkylated human AGT structures: a novel zinc site, inhibitor and extrahelical base binding. EMBO J 2000; 19:1719-1730.
80. Hashimoto H, Inoue T, Nishioka M, Fujiwara S, Takagi M, Imanaka T, Kai Y. Hyperthermostable protein structure maintained by intra and inter-helix ion-pairs in archaeal O6-methylguanine-DNA methyltransferase. J Mol Biol 1999; 292:707-716.
81. Lin Y, Dotsch V, Wintner T, Peariso K, Myers LC, Penner-Hahn JE, Verdine GL, Wagner G. Structural basis for the functional switch of the E. coli Ada protein. Biochemistry 2001; 40:4261-4271.
82. Moore MH, Gulbis JM, Dodson EJ, Demple B, Moody PC. Crystal structure of a suicidal DNA repair protein: the Ada O6-methylguanine-DNA methyltransferase from E. coli. EMBO J 1994; 13:1495-1501.
83. Trewick SC, Henshaw TF, Hausinger RP, Lindahl T, Sedgwick B. Oxidative demethy-lation by Escherichia coli AlkB directly reverts DNA base damage. Nature 2002; 419:174-178.
84. Falnes PO, Johansen RF, Seeberg E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 2002; 419:178-182.
85. Aravind L, Koonin EV. The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol 2001; 2: RESEAR CH0007.
86. Aas PA, Otterlei M, Falnes PO, Vagbo CB, Skorpen F, Akbari M, Sundheim O, Bjoras M, Slupphaug G, Seeberg E, Krokan HE. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 2003; 421: 859-863.
87. Lau AY, Wyatt MD, Glassner BJ, Samson LD, Ellenberger T. Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proc Natl Acad Sci USA 2000; 97:13573-13578.
88. Brennan RG, Matthews BW. The helix-turn-helix DNA binding motif. J Biol Chem 1989; 264:1903-1906.
89. Lindahl T. Repair of intrinsic DNA lesions. Mutat Res 1990; 238:305-311.
90. Barzilay G, Hickson ID. Structure and function of apurinic/apyrimidinic endonucleases. Bioessays 1995; 17:713-719.
91. Demple B, Harrison L. Repair of oxidative damage to DNA: enzymology and biology. Annu Rev Biochem 1994; 63:915-948.
92. Ramotar D. The apurinic-apyrimidinic endonuclease IV family of DNA repair enzymes. Biochem Cell Biol 1997; 75:327-336.
93. Ljungquist S, Lindahl T, Howard-Flanders P. Methyl methane sulfonate-sensitive mutant of Escherichia coli deficient in an endonuclease specific for apurinic sites in deoxyribonucleic acid. J Bacteriol 1976; 126:646-653.
94. Yajko DM, Weiss B. Mutations simultaneously affecting endonuclease II and exonuclease III in Escherichia coli. Proc Natl Acad Sci USA 1975; 72:688-692.
95. Ljungquist S. A new endonuclease from Escherichia coli acting at apurinic sites in DNA. J Biol Chem 1977; 252:2808-2814.
96. Xanthoudakis S, Smeyne RJ, Wallace JD, Curran T. The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc Natl Acad Sci USA 1996; 93:8919-8923.
97. Bennett RA, Wilson DM, 3rd, Wong D, Demple B. Interaction of human apurinic endonuclease and DNA polymerase beta in the base excision repair pathway. Proc Natl Acad Sci USA 1997; 94:7166-7169.
98. Vidal AE, Boiteux S, Hickson ID, Radicella JP. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J 2001; 20:6530-6539.
99. Dianova, II, Bohr VA, Dianov GL. Interaction of human AP endonuclease 1 with flap endonuclease 1 and proliferating cell nuclear antigen involved in long-patch base excision repair. Biochemistry 2001; 40:12639-12644.
100. Ranalli TA, Tom S, Bambara RA. AP endonuclease 1 coordinates flap endonuclease 1 and DNA ligase I activity in long patch base excision repair. J Biol Chem 2002; 27:27.
101. Xanthoudakis S, Miao G, Wang F, Pan YC, Curran T. Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO J 1992; 11: 3323-3335.
102. Tell G, Zecca A, Pellizzari L, Spessotto P, Colombatti A, Kelley MR, Damante G, Pucillo C. An ‘environment to nucleus’ signaling system operates in B lymphocytes: redox status modulates BSAP/Pax-5 activation through Ref-1 nuclear translocation. Nucleic Acids Res 2000; 28:1099-1105.
103. Tell G, Pellizzari L, Cimarosti D, Pucillo C, Damante G. Ref-1 controls pax-8 DNA-binding activity. Biochem Biophys Res Commun 1998; 252:178-183.
104. Jayaraman L, Murthy KG, Zhu C, Curran T, Xanthoudakis S, Prives C. Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes Dev 1997; 11:558-570.
105. Mol CD, Kuo CF, Thayer MM, Cunningham RP, Tainer JA. Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 1995; 374:381-386.
106. Mol CD, Izumi T, Mitra S, Tainer JA. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination. Nature 2000; 403:451-456.
107. Levin JD, Shapiro R, Demple B. Metalloenzymes in DNA repair. Escherichia coli endonuclease IV and Saccharomyces cerevisiae Apn1. J Biol Chem 1991; 266:22893-22898.
108. Hosfield DJ, Guan Y, Haas BJ, Cunningham RP, Tainer JA. Structure of the DNA repair enzyme endonuclease IV and its DNA complex: double-nucleotide flipping at abasic sites and three-metal-ion catalysis. Cell 1999; 98:397-408.
109. Haas BJ, Sandigursky M, Tainer JA, Franklin WA, Cunningham RP. Purification and characterization of Thermotoga maritima endonuclease IV, a thermostable apurinic/apyrimidinic endonuclease and 3’-repair diesterase. J Bacteriol 1999; 181:2834-2839.
110. Ide H, Tedzuka K, Shimzu H, Kimura Y, Purmal AA, Wallace SS, Kow YW. Alpha-deoxyadenosine, a major anoxic radiolysis product of adenine in DNA, is a substrate for Escherichia coli endonuclease IV. Biochemistry 1994; 33:7842-7847.
111. Ischenko AA, Saparbaev MK. Alternative nucleotide incision repair pathway for oxidative DNA damage. Nature 2002; 415:183-187.
112. Ocampo MT, Chaung W, Marenstein DR, Chan MK, Altamirano A, Basu AK, Boorstein RJ, Cunningham RP, Teebor GW. Targeted deletion of mNth1 reveals a novel DNA repair enzyme activity. Mol Cell Biol 2002; 22:6111-6121.
113. Blaisdell JO, Wallace SS. Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. Proc Natl Acad Sci USA 2001; 98:7426-7430.