The intricate structural chemistry of base excision repair machinery: Implications for DNA damage recognition, removal, and repair

DNA Repair

Volumn 6, Issue 4, 2007, Pages 410-428

  Hitomi, Kenichi ^a,b,c   Iwai, Shigenori ^a   Tainer, John A ^b,c  

^a OSAKA UNIVERSITY   (Japan)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Base excision; Base excision repair pathway; Crystallography; Damage recognition; Damage reversal; DNA damage; DNA repair; Enzyme DNA complex; FEN 1; Genome maintenance; Glycosylase; Ligase; N glycosylase AP lyase enzymes; PCNA; Polymerase; Structure specific nuclease

Indexed keywords

DNA BASE; DNA GLYCOSYLTRANSFERASE; DNA POLYMERASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE;

ARTICLE; DNA DAMAGE; DNA PROTEIN COMPLEX; DNA REPAIR; DNA STRUCTURE; EXCISION REPAIR; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; DNA; DNA DAMAGE; DNA REPAIR; DNA REPAIR ENZYMES; HUMANS; PROTEIN CONFORMATION; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; ZINC;

EID: 33847673237     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.10.004     Document Type: Article

References (145)

1. Denver D.R., Swenson S.L., and Lynch M. An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases. Mol. Biol. Evol. 20 (2003) 1603-1611
2. Krokan H.E., Standal R., and Slupphaug G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 325 (1997) 1-16
3. Lindahl T., and Wood R.D. Quality control by DNA repair. Science 286 (1999) 1897-1905
4. Demple B., and Harrison L.B. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63 (1994) 915-948
5. Wood R.D. DNA repair in eukaryotes. Annu. Rev. Biochem. 65 (1996) 135-167
6. Huffman J.L., Sundheim O., and Tainer J.A. DNA base damage recognition and removal: new twists and grooves. Mutat. Res. 577 (2005) 55-76
7. Izumi T., Wiederhold L.R., Roy G., Roy R., Jaiswal A., Bhakat K.K., Mitra S., and Hazra T.K. Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage. Toxicology 193 (2003) 43-65
8. Boiteux S., and Guillet M. Abasic sites in DNA: repair and biological consequences in Saccharomyces cerevisiae. DNA Repair (Amst) 3 (2004) 1-12
9. Sobol R.W., Kartalou M., Almeida K.H., Joyce D.F., Engelward B.P., Horton J.K., Prasad R., Samson L.D., and Wilson S.H. Base excision repair intermediates induce p53-independent cytotoxic and genotoxic responses. J. Biol. Chem. 278 (2003) 39951-39959
10. Kavli B., Slupphaug G., Mol C.D., Arvai A.S., Peterson S.B., Tainer J.A., and Krokan H.E. Excision of cytosine and thymine from DNA by mutants of human uracil-DNA glycosylase. EMBO J. 15 (1996) 3442-3447
11. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
12. Mol C.D., Arvai A.S., Slupphaug G., Kavli B., Alseth I., Krokan H.E., and Tainer J.A. Crystal structure and mutational analysis of human uracil-DNA glycosylase: structural basis for specificity and catalysis. Cell 80 (1995) 869-878
13. Slupphaug G., Mol C.D., Kavli B., Arvai A.S., Krokan H.E., and Tainer J.A. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 384 (1996) 87-92
14. McMurray C.T., and Tainer J.A. Cancer, cadmium and genome integrity. Nat. Genet. 34 (2003) 239-241
15. Thayer M.M., Ahern H., Xing D., Cunningham R.P., and Tainer J.A. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J. 14 (1995) 4108-4120
16. Hosfield D.J., Mol C.D., Shen B., and Tainer J.A. Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: coupling DNA and PCNA binding to FEN-1 activity. Cell 95 (1998) 135-146
17. Kuo C.F., McRee D.E., Fisher C.L., O'Handley S.F., Cunningham R.P., and Tainer J.A. Atomic structure of the DNA repair [4Fe-4S] enzyme endonuclease III. Science 258 (1992) 434-440
18. Guan Y., Manuel R.C., Arvai A.S., Parikh S.S., Mol C.D., Miller J.H., Lloyd R.S., and Tainer J.A. MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat. Struct. Biol. 5 (1998) 1058-1064
19. Mol C.D., Arvai A.S., Begley T.J., Cunningham R.P., and Tainer J.A. Structure and activity of a thermostable thymine-DNA glycosylase: evidence for base twisting to remove mismatched normal DNA bases. J. Mol. Biol. 315 (2002) 373-384
20. Hollis T., Ichikawa Y., and Ellenberger T. DNA bending and a flip-out mechanism for base excision by the helix-hairpin-helix DNA glycosylase, Escherichia coli AlkA. EMBO J. 19 (2000) 758-766
21. Bruner S.D., Norman D.P., and Verdine G.L. Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature 403 (2000) 859-866
22. Volk D.E., House P.G., Thiviyanathan V., Luxon B.A., Zhang S., Lloyd R.S., and Gorenstein D.G. Structural similarities between MutT and the C-terminal domain of MutY. Biochemistry 39 (2000) 7331-7336
23. Hendrich B., Hardeland U., Ng H.-H., Jiricny J., and Bird A. The thymine glycosylase MBD4 can bind to the product of deamination at methylated CpG sites. Nature 401 (1999) 301-304
24. Petronzelli F., Riccio A., Markham G.D., Seeholzer S.H., Genuardi M., Karbowski M., Yeung A.T., Matsumoto Y., and 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. 185 (2000) 473-480
25. Parikh S.S., Walcher G., Jones G.D., Slupphaug G., Krokan H.E., Blackburn G.M., and Tainer J.A. Uracil-DNA glycosylase-DNA substrate and product structures: conformational strain promotes catalytic efficiency by coupled stereoelectronic effects. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 5083-5088
26. Ohki I., Shimotake N., Fujita N., Jee J.-G., Ikegami T., Nakao M., and Shirakawa M. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105 (2001) 487-497
27. Wakefield R.I.D., Smith B.O., Nan X., Free A., Soteriou A., Uhrin D., Bird A.P., and Barlow P.N. The solution structure of the domain from MeCP2 that binds to methylated DNA. J. Mol. Biol. 291 (1999) 1055-1065
28. Petronzelli F., Riccio A., Markham G.D., Seeholzer S.H., Stoerker J., Genuardi M., et al. Biphasic kinetics of the human DNA repair protein MED1 (MBD4), a mismatch-specific DNA N-glycosylase. J. Biol. Chem. 275 (2000) 32422-32429
29. Parikh S.S., Mol C.D., Slupphaug G., Bharati S., Krokan H.E., and Tainer J.A. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 17 (1998) 5214-5226
30. Fromme J.C., Banerjee A., Huang S.J., and Verdine G.L. Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature 427 (2004) 652-656
31. Michaels M.L., and Miller J.H. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174 (1992) 6321-6325
32. Mildvan A.S., Weber D.J., and Abeygunawardana C. Solution structure and mechanism of the MutT pyrophosphohydrolase. Adv. Enzymol. Relat. Areas Mol. Biol. 73 (1999) 183-207
33. Gogos A., Cillo J., Clarke N.D., and Lu A.-L. Specific recognition of A/G and A/7,8-dihydro-8-oxoguanine (8-oxoG) mismatches by Escherichia coli MutY: removal of the C-terminal domain preferentially affects A/8-oxoG recognition. Biochemistry 35 (1996) 16665-16671
34. Noll D.M., Gogos A., Granek J.A., and Clarke N.D. 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 38 (1999) 6374-6379
35. Fromme J.C., and Verdine G.L. Structure of a trapped endonuclease III-DNA covalent intermediate. EMBO J. 22 (2003) 3461-3471
36. Massiah M.A., Saraswat V., Azurmendi H.F., and Mildvan A.S. Solution structure and NH exchange studies of the MutT pyrophosphohydrolase complexed with Mg(2+) and 8-oxo-dGMP, a tightly bound product. Biochemistry 42 (2003) 10140-10154
37. Al-Tassan N., Chmiel N.H., Maynard J., Fleming N., Livingston A.L., Williams G.T., Hodges A.K., Davies D.R., David S.S., Sampson J.R., and Cheadle J.P. Inherited variants of MYH associated with somatic G:C → T:A mutations in colorectal tumors. Nat. Genet. 30 (2002) 227-232
38. Chmiel N.H., Livingston A.L., and David S.S. Insight into the functional consequences of inherited variants of the hMYH adenine glycosylase associated with colorectal cancer: complementation assays with hMYH variants and pre-steady-state kinetics of the corresponding mutated E. coli enzymes. J. Mol. Biol. 327 (2003) 431-443
39. Brown T.C., and Jiricny J. A specific mismatch repair event protects mammalian cells from loss of 5-methylcytosine. Cell 50 (1987) 945-950
40. Hardeland U., Bentele M., Lettieri T., Steinacher R., Jiricny J., and Schar P. Thymine DNA glycosylase. Prog. Nucleic Acid Res. Mol. Biol. 68 (2001) 235-253
41. Gallinari P., and Jiricny J. A new class of uracil-DNA glycosylases related to human thymine-DNA glycosylase. Nature 383 (1996) 735-738
42. Barrett T.E., Savva R., Panayotou G., Barlow T., Brown T., Jiricny J., and Pearl L.H. Crystal structure of a G:T/U mismatch-specific DNA glycosylase: mismatch recognition by complementary-strand interactions. Cell 92 (1998) 117-129
43. Pearl L.H. Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res. 460 (2000) 165-181
44. Barrett T.E., Scharer O.D., Savva R., Brown T., Jiricny J., Verdine G.L., and Pearl L.H. Crystal structure of a thwarted mismatch glycosylase DNA repair complex. EMBO J. 18 (1999) 6599-6609
45. Hardeland U., Steinacher R., Jiricny J., and Schar P. Modification of the human thymine-DNA glycosylase by ubiquitin-like proteins facilitates enzymatic turnover. EMBO J. 21 (2002) 1456-1464
46. Steinacher R., and Schar P. Functionality of human thymine DNA glycosylase requires SUMO-regulated changes in protein conformation. Curr. Biol. 15 (2005) 616-623
47. Baba D., Maita N., Jee J.G., Uchimura Y., Saitoh H., Sugasawa K., Hanaoka F., Tochio H., Hiroaki H., and Shirakawa M. Crystal structure of thymine DNA glycosylase conjugated to SUMO-1. Nature 435 (2005) 979-982
48. Song J., Durri L.K., Wilkinson T.A., Krontiris T.G., and Chen Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 14373-14378
49. Bjørås M., Seeberg E., Luna L., Pearl L.H., and Barrett T.E. Reciprocal "flipping" underlies substrate recognition and catalytic activation by the human 8-oxo-guanine DNA glycosylase. J. Mol. Biol. 317 (2002) 171-177
50. Norman D.P., Chung S.J., and Verdine G.L. Structural and biochemical exploration of a critical amino acid in human 8-oxoguanine glycosylase. Biochemistry 42 (2003) 1564-1572
51. Fromme J.C., Bruner S.D., Yang W., Karplus M., and Verdine G.L. Product-assisted catalysis in base-excision DNA repair. Nat. Struct. Biol. 10 (2003) 204-211
52. Chung S.J., and Verdine G.L. Structures of end products resulting from lesion processing by a DNA glycosylase/lyase. Chem. Biol. 11 (2004) 1643-1649
53. Banerjee A., Yang W., Karplus M., and Verdine G.L. Structure of a repair enzyme interrogating undamaged DNA elucidates recognition of damaged DNA. Nature 434 (2005) 612-618
54. Tchou J., Kasai H., Shibutani S., Chung M.H., Laval J., Grollman A.P., and Nishimura S. 8-Oxoguanine (8-hydroxyguanine) DNA glycosylase and its substrate specificity. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 4690-4694
55. Park J., Chen L., Tockman M.S., Elahi A., and Lazarus P. The human 8-oxoguanine DNA N-glycosylase 1 (hOGG1) DNA repair enzyme and its association with lung cancer risk. Pharmacogenetics 14 (2004) 103-109
56. Le Marchand L., Donlon T., Lum-Jones A., Seifried A., and Wilkens L.R. Association of the hOGG1 Ser326Cys polymorphism with lung cancer risk. Cancer Epidemiol. Biomarkers Prev. 11 (2002) 409-412
57. Morland I., Luna L., Gustad E., Seeberg E., and Bjoras M. Product inhibition and magnesium modulate the dual reaction mode of hOgg1. DNA Repair (Amst) 4 (2005) 381-387
58. Sugahara M., Mikawa T., Kumasaka T., Yamamoto M., Kato R., Fukuyama K., Inoue Y., and Kuramitsu S. Crystal structure of a repair enzyme of oxidatively damaged DNA, MutM (Fpg), from an extreme thermophile, Thermus thermophilus HB8. EMBO J. 19 (2000) 3857-3869
59. Fromme J.C., and Verdine G.L. Structural insights into lesion recognition and repair by the bacterial 8-oxoguanine DNA glycosylase MutM. Nat. Struct. Biol. 9 (2002) 544-552
60. Gilboa R., Zharkov D.O., Golan G., Fernandes A.S., Gerchman S.E., Matz E., Kycia J.H., Grollman A.P., and Shoham G. Structure of formamidopyrimidine-DNA glycosylase covalently complexed to DNA. J. Biol. Chem. 277 (2002) 19811-19816
61. Zharkov D.O., Golan G., Gilboa R., Fernandes A.S., Gerchman S.E., Kycia J.H., Rieger R.A., Grollman A.P., and Shoham G. Structural analysis of an Escherichia coli endonuclease VIII covalent reaction intermediate. EMBO J. 21 (2002) 789-800
62. Serre L., Pereira de Jesus K., Boiteux S., Zelwer C., and Castaing B. Crystal structure of the Lactococcus lactis formamidopyrimidine-DNA glycosylase bound to an abasic site analogue-containing DNA. EMBO J. 21 (2002) 2854-2865
63. Fromme J.C., and Verdine G.L. DNA lesion recognition by the bacterial repair enzyme MutM. J. Biol. Chem. 278 (2003) 51543-51548
64. Coste F., Ober M., Carell T., Boiteux S., Zelwer C., and Castaing B. Structural basis for the recognition of the FapydG lesion (2,6-diamino-4-hydroxy-5-formamidopyrimidine) by formamidopyrimidine-DNA glycosylase. J. Biol. Chem. 279 (2004) 44074-44083
65. Doublie S., Bandaru V., Bond J.P., and Wallace S.S. The crystal structure of human endonuclease VIII-like 1 (NEIL1) reveals a zincless finger motif required for glycosylase activity. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 10284-10289
66. Golan G., Zharkov D.O., Feinberg H., Fernandes A.S., Zaika E.I., Kycia J.H., Grollman A.P., and Shoham G. Structure of the uncomplexed DNA repair enzyme endonuclease VIII indicates significant interdomain flexibility. Nucleic Acids Res. 33 (2005) 5006-5016
67. Boiteux S., Gajewski E., Laval J., and Dizdaroglu M. Substrate specificity of the Escherichia coli Fpg protein (formamidopyrimidine-DNA glycosylase): excision of purine lesions in DNA produced by ionizing radiation or photosensitization. Biochemistry 31 (1992) 106-110
68. Miller H., Fernandes A.S., Zaika E., McTigue M.M., Torres M.C., Wente M., Iden C.R., and Grollman A.P. Stereoselective excision of thymine glycol from oxidatively damaged DNA. Nucleic Acids Res. 32 (2004) 338-345
69. Katafuchi A., Nakano T., Masaoka A., Terato H., Iwai S., Hanaoka F., and Ide H. Differential specificity of human and Escherichia coli endonuclease III and VIII homologues for oxidative base lesions. J. Biol. Chem. 279 (2004) 14464-14471
70. Dou H., Mitra S., and Hazra T.K. Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem. 278 (2003) 49679-49684
71. Das A., Rajagopalan L., Mathura V.S., Rigby S.J., Mitra S., and Hazra T.K. Identification of a zinc finger domain in the human NEIL2 (Nei-like-2) protein. J. Biol. Chem. 279 (2004) 47132-47138
72. Wiederhold L., Leppard J.B., Kedar P., Karimi-Busheri F., Rasouli-Nia A., Weinfeld M., Tomkinson A.E., Izumi T., Prasad R., Wilson S.H., Mitra S., and Hazra T.K. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 15 (2004) 209-220
73. Pegg A.E. Repair of O(6)-alkylguanine by alkyltransferases. Mutat. Res. 462 (2000) 83-100
74. Moore M.H., Gulbis J.M., Dodson E.J., Demple B., and Moody P.C. Crystal structure of a suicidal DNA repair protein: the Ada O6-methylguanine-DNA methyltransferase from E. coli. EMBO J. 13 (1994) 1495-1501
75. Hashimoto H., Inoue T., Nishioka M., Fujiwara S., Takagi M., Imanaka T., and Kai Y. Hyperthermostable protein structure maintained by intra and inter-helix ion-pairs in archaeal O6-methylguanine-DNA methyltransferase. J. Mol. Biol. 292 (1999) 707-716
76. Daniels D.S., Mol C.D., Arvai A.S., Kanugula S., Pegg A.E., and Tainer J.A. Active and alkylated human AGT structures: a novel zinc site, inhibitor and extrahelical base binding. EMBO J. 19 (2000) 1719-1730
77. Wibley J.E., Pegg A.E., and Moody P.C. Crystal structure of the human O(6)-alkylguanine-DNA alkyltransferase. Nucleic Acids Res. 28 (2000) 393-401
78. Daniels D.S., Woo T.T., Luu K.X., Noll D.M., Clarke N.D., Pegg A.E., and Tainer J.A. DNA binding and nucleotide flipping by the human DNA repair protein AGT. Nat. Struct. Mol. Biol. 11 (2004) 714-720
79. Duguid E.M., Rice P.A., and He C. The structure of the human AGT protein bound to DNA and its implications for damage detection. J. Mol. Biol. 350 (2005) 657-666
80. Wintjens R., and Rooman M. Structural classification of HTH DNA-binding domains and protein-DNA interaction modes. J. Mol. Biol. 262 (1996) 294-313
81. Hosfield D.J., Guan Y., Haas B.J., Cunningham R.P., and Tainer J.A. Structure of the DNA repair enzyme endonuclease IV and its DNA complex: double-nucleotide flipping at abasic sites and three-metal-ion catalysis. Cell 98 (1999) 397-408
82. Mol C.D., Izumi T., Mitra S., and Tainer J.A. DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination. Nature 403 (2000) 451-456
83. Rasimas J.J., Kanugula S., Dalessio P.M., Ropson I.J., Fried M.G., and Pegg A.E. Effects of zinc occupancy on human O6-alkylguanine-DNA alkyltransferase. Biochemistry 42 (2003) 980-990
84. Myers L.C., Terranova M.P., Ferentz A.E., Wagner G., and Verdine G.L. Repair of DNA methylphosphotriesters through a metalloactivated cysteine nucleophile. Science 261 (1993) 1164-1167
85. He C., Hus J., Sun L., Zhou P., Norman D., Dötsch V., Wei H., Gross J., Lane W., and Wagner G. A methylation-dependent electrostatic switch controls DNA repair and transcriptional activation by Ada. Mol. Cell 20 (2005) 117-129
86. Arvind L., and Koonin E.V. The DNA repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2 (2001) 0007.1-0007.8
87. Trewick S.C., Henshaw T.F., Hausinger R.P., Lidahl T., and Sedgwick B. Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature 419 (2002) 174-178
88. Falnes P.Ø., Johansen R.F., and Seeberg E. AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature 419 (2002) 178-182
89. Duncan T., Trewick S.C., Koivisto P., Bates P.A., Lindahl T., and Sedgwick B. Reversal of DNA alkylation damage by two human dioxygenases. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 16660-16665
90. Aas P.A., Otterlei M., Falnes P.Ø., Vågbø C.B., Skorpen F., Akbari M., Sundheim O., Bjørås M., Slupphaug G., Seeberg E., and Krokan H.E. Human and bacterial oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421 (2003) 859-863
91. Falnes P.Ø. Repair of 3-methylthymine and 1-methylguanine lesions by bacterial and human AlkB proteins. Nucleic Acids Res. 32 (2004) 6260-6267
92. Mishina Y., Yang C.G., and He C. Direct repair of the exocyclic DNA adduct 1,N6-ethenoadenine by the DNA repair AlkB proteins. J. Am. Chem. Soc. 127 (2005) 14594-14595
93. Delaney J.C., Smeester L., Wong C., Frick L.E., Taghizadeh K., Wishnok J.S., Drennan C.L., Samson L.D., and Essigmann J.M. AlkB reverses etheno DNA lesions caused by lipid oxidation in vitro and in vivo. Nat. Struct. Mol. Biol. 12 (2005) 855-860
94. Mishina Y., and He C. Probing the structure and function of the Escherichia coli DNA alkylation repair AlkB protein through chemical cross-linking. J. Am. Chem. Soc. 125 (2003) 8730-8731
95. Falnes P.Ø., Bjørås M., Aas P.A., Sundheim O., and Seeberg E. Substrate specificities of bacterial and human AlkB proteins. Nucleic Acids Res. 32 (2004) 3456-3461
96. Mishina Y., Lee C.-H.J., and He C. Interaction of human and bacterial AlkB proteins with DNA as probed through chemical cross-linking studies. Nucleic Acids Res. 32 (2004) 1548-1554
97. Yu B., Edstrom W.C., Benach J., Hamuro Y., Weber P.C., Gibney B.R., and Hunt J.F. Crystal structures of catalytic complexes of the oxidative DNA/RNA repair enzyme AlkB. Nature 439 (2006) 879-884
98. Hausinger R.P. FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes. Crit. Rev. Biochem. Mol. Biol. 39 (2004) 21-68
99. Sundheim O., Vågbø C.B., Bjørås M., Sousa M.M.L., Talstad V., Aas P.A., Drabløs F., Krokan H.E., Tainer J.A., and Slupphaug G. Human ABH3 structure and key residues for oxidative demethylation to reverse DNA/RNA damage. EMBO J. 25 (2006) 3389-3397
100. Kubota Y., Nash R.A., Klungland A., et al. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein. EMBO J. 15 (1996) 6662-6670
101. Jónsson Z.O., Hindges R., and Hübscher U. Regulation of DNA replication and repair proteins through interaction with the front side of proliferating cell nuclear antigen. EMBO J. 17 (1998) 2412-2425
102. Hwang K.Y., Baek K., Kim H.-Y., and Cho Y. The crystal structure of flap endonuclease-1 from Methanococcus jannaschii. Nat. Struct. Biol. 5 (1998) 707-713
103. Chapados B., Hosfield D., Han S., Qiu J., Yelent B., Shen B., and Tainer J. Structural basis for FEN-1 substrate specificity and PCNA-mediated activation in DNA replication and repair. Cell 116 (2004) 39-50
104. Sakurai S., Kitano K., Yamaguchi H., Hamada K., Okada K., Fukuda K., Uchida M., Ohtsuka E., Morioka H., and Hakoshima T. Structural basis for recruitment of human flap endonuclease 1 to PCNA. EMBO J. 24 (2005) 683-693
105. Krishna T.S.R., Kong X.-P., Gary S., Burgers P.M., and Kuriyan J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79 (1994) 1233-1243
106. Sobol R.W., Horton J.K., Kuhn R., et al. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 379 (1996) 183-186
107. Jay II F.D., Robert J.A., Zuzana H., Rose A.F., and Zdenek H. 2.3 A crystal structure of the catalytic domain of DNA polymerase beta. Cell 76 (1994) 1123-1133
108. Pelletier H., Sawaya M.R., Kumar A., Wilson S.H., and Kraut J. Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP. Science 264 (1994) 1891-1903
109. Sawaya M.R., Pelletier H., Kumar A., Wilson S.H., and Kraut J. Crystal structure of rat DNA polymerase beta: evidence for a common polymerase mechanism. Science 264 (1994) 1930-1935
110. Pelletier H., Sawaya M.R., Wolfle W., Wilson S.H., and Kraut J. Crystal structures of human DNA polymerase beta complexed with DNA: implications for catalytic mechanism, processivity, and fidelity. Biochemistry 35 (1996) 12742-12761
111. Sawaya M.R., Prasad R., Wilson S.H., Kraut J., and Pelletier H. Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 36 (1997) 11205-11215
112. Arndt J.W., Gong W., Zhong X., Showalter A.K., Liu J., Dunlap C.A., Lin Z., Paxson C., Tsai M.D., and Chan M.K. Insight into the catalytic mechanism of DNA polymerase beta: structures of intermediate complexes. Biochemistry 40 (2001) 5368-5375
113. Krahn J., Beard W., Miller H., Grollman A., and Wilson S. Structure of DNA polymerase beta with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential. Structure 11 (2003) 121-127
114. Krahn J.M., Beard W.A., and Wilson S.H. Structural insights into DNA polymerase beta deterrents for misincorporation support an induced-fit mechanism for fidelity. Structure 12 (2004) 1823-1832
115. Johnson S., and Beese L. Structures of mismatch replication errors observed in a DNA polymerase. Cell 116 (2004) 803-816
116. Batra V.K., Beard W.A., Shock D.D., Pedersen L.C., and Samuel H.W. Nucleotide-induced DNA polymerase active site motions accommodating a mutagenic DNA intermediate. Structure 13 (2005) 1225-1233
117. Matsumoto Y., and Kim K. Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair. Science 269 (1995) 699-702
118. Prasad R., Batra V.K., Yang X.-P., Krahn J.M., Pedersen L.C., Beard W.A., and Wilson S.H. Structural insight into the DNA polymerase P deoxyribose phosphate lyase mechanism. DNA repair (Amst) 4 (2005) 1347-1357
119. Tomkinson A.E., Vijayakumar S., Pascal J.M., and Ellenberger T. DNA ligases: structure, reaction mechanism, and function. Chem. Rev. 106 (2006) 687-699
120. Mackey Z.B., Niedergang C., Murcia J.M., Leppard J., Au K., Chen J., Murcia G., and Tomkinson A.E. DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly(ADP-ribose) polymerase. J. Biol. Chem. 274 (1999) 21679-21687
121. Kulczyk A.W., Yang J.C., and Neuhaus D. Solution structure and DNA binding of the zinc-finger domain from DNA ligase IIIα. J. Mol. Biol. 341 (2004) 723-738
122. Satoh M.S., and Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature 356 (1992) 356-358
123. Krishnan V.V., Thornton K.H., Thelen M.P., and Cosman M. Solution structure and backbone dynamics of the human DNA ligase III BRCT domain. Biochemistry 40 (2001) 13158-13166
124. Tomkinson A.E., and Levin D.S. Mammalian DNA ligase. BioEssay 19 (1997) 893-901
125. Ramos W., Tappe N., Talamantez J., Friedberg E.C., and Tomkinson A.E. Two distinct DNA ligase activities in mitotic extracts of the yeast Saccharomyces cerevisiae. Nucleic Acids Res. 25 (1997) 1485-1492
126. Zhang X., Morera S., Bates P.A., Whitehead P.C., Coffer A.I., Hainbucher K., et al. Structure of an XRCC1 BRCT domain: a new protein-protein interaction module. EMBO J. 17 (1998) 6404-6411
127. Pascal J.M., O'Brien P.J., Tomkinson A.E., and Ellenberger T. Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 432 (2004) 473-478
128. Nishida H., Kiyonari S., Ishino Y., and Morikawa K. The closed structure of an archaeal DNA ligase from Pyrococcus furiosus. J. Mol. Biol. 360 (2006) 956-967
129. Mol C.D., Arvai A.S., Sanderson R.J., Slupphaug G., Kavli B., Krokan H.E., Mosbaugh D.W., and Tainer J.A. Crystal structure of human uracil-DNA glycosylase in complex with a protein inhibitor: protein mimicry of DNA. Cell 82 (1995) 701-708
130. Putnam C.D., Shroyer M.J.N., Lundquist A.J., Mol C.D., Arvai A.S., Mosbaugh D.W., and Tainer J.A. Protein mimicry of DNA from crystal structures of the uracil-DNA glycosylase inhibitor protein and its complex with Escherichia coli uracil-DNA glycosylase. J. Mol. Biol. 287 (1999) 331-346
131. Putnam C.D., and Tainer J.A. Protein mimicry of DNA and pathway regulation. DNA Repair (Amst) 4 (2005) 1410-1420
132. Sarker A., Tsutakawa S., Kostek S., Ng C., Shin D., Peris M., Campeau E., Tainer J., Nogales E., and Cooper P. Recognition of RNA polymerase II and transcription bubbles by XPG, CSB, and TFIIH: insights for transcription-coupled repair and Cockayne Syndrome. Mol. Cell 20 (2005) 187-198
133. Putnam C.D., Clancy S.B., Tsuruta H., Gonzalez S., Wetmur J.G., and Tainer J.A. Structure and mechanism of the RuvB Holliday junction branch migration motor. J. Mol. Biol. 311 (2001) 297-310
134. Hopfner K., Karcher A., Shin D., Craig L., Arthur L., Carney J., and Tainer J. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101 (2000) 789-800
135. Williams R.S., and Tainer J.A. A nanomachine for making ends meet: MRN is a flexing scaffold for the repair of DNA double-strand breaks. Mol. Cell 19 (2005) 724-726
136. Shin D.S., Pellegrini L., Daniels D.S., Yelent B., et al. Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J. 22 (2003) 4566-4576
137. Otterlei M., Kavli B., Standal R., Skjelbred C., Bharati S., and Krokan H.E. Repair of chromosomal abasic sites in vivo involves at least three different repair pathways. EMBO J. 19 (2000) 5542-5551
138. Chao E.C., and Lipkin S.M. Molecular models for the tissue specificity of DNA mismatch repair-deficient carcinogenesis. Nucleic Acids Res. 34 (2006) 840-852
139. de Boer J., and Hoeijmakers J.H. Nucleotide excision repair and human syndromes. Carcinogenesis 21 (2000) 453-460
140. J.J. Perry, L. Fan, J.A. Tainer, Developing master keys to brain pathology, cancer and aging from the structural biology of proteins controlling reactive oxygen species and DNA repair, Neuroscience (2006) Epub ahead of print.
141. Doi Y., Katafuchi A., Fujiwara Y., Hitomi K., Tainer J.A., Ide H., and Iwai S. Synthesis and characterization of oligonucleotides containing 2′-fluorinated thymidine glycol as inhibitors of the endonuclease III reaction. Nucleic Acids Res. 34 (2006) 1540-1551
142. Pascal J.M., Tsodikov O.V., Hura G.L., Song W., Cotner E.A., Classen S., Tomkinson A.E., Tainer J.A., and Ellenberger T. A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA. Mol. Cell 24 (2006) 279-291
143. S. Vijayakumar, B.R. Chapados, K.H. Schmidt, R.D. Kolodner, J.A. Tainer, A.E. Tomkinson, The C-terminal domain of yeast PCNA is required for physical and functional interactions with Cdc9 DNA ligase, Nucleic Acids Res. (2007) in press.
144. Fan L., Kim S., Farr C.L., Schaefer K.T., Randolph K.M., Tainer J.A., and Kaguni L.S. A novel processive mechanism for DNA synthesis revealed by structure, modeling and mutagenesis of the accessory subunit of human mitochondrial DNA polymerase. J. Mol. Biol. 358 (2006) 1229-1243
145. Ivanov I., Chapados B.R., McCammon J.A., and Tainer J.A. Proliferating cell nuclear antigen loaded onto double-stranded DNA: dynamics, minor groove interactions and functional implications. Nucleic Acids Res. 34 (2006) 6023-6033