Structure of the E. coli DNA Glycosylase AlkA Bound to the Ends of Duplex DNA: A System for the Structure Determination of Lesion-Containing DNA

Structure

Volumn 16, Issue 8, 2008, Pages 1166-1174

  Bowman, Brian R ^a   Lee, Seongmin ^a   Wang, Shuyu ^a   Verdine, Gregory L ^a,b,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

DNA; PROTEIN

Indexed keywords

1,N6 ETHENOADENINE; 8 HYDROXYGUANINE; ADENINE; DEOXYINOSINE; DNA GLYCOSYLASE ALKA; DNA GLYCOSYLTRANSFERASE; DOUBLE STRANDED DNA;

ARTICLE; DNA BINDING; DNA DAMAGE; DNA DETERMINATION; DNA MODIFICATION; DNA STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DNA; DNA DAMAGE; DNA GLYCOSYLASES; ESCHERICHIA COLI; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEOTIDES; PROTEIN CONFORMATION;

EID: 48149108427     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2008.04.012     Document Type: Article

References (65)

1. Banerjee A., and Verdine G.L. A nucleobase lesion remodels the interaction of its normal neighbor in a DNA glycosylase complex. Proc. Natl. Acad. Sci. USA 103 (2006) 15020-15025
2. 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
3. Banerjee A., Santos W.L., and Verdine G.L. Structure of a DNA glycosylase searching for lesions. Science 311 (2006) 1153-1157
4. Barrett T.E., Savva R., Barlow T., Brown T., Jiricny J., and Pearl L.H. Structure of a DNA base-excision product resembling a cisplatin inter-strand adduct. Nat. Struct. Biol. 5 (1998) 697-701
5. 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
6. Barrio J.R., Secrist III J.A., and Leonard N.J. Fluorescent adenosine and cytidine derivatives. Biochem. Biophys. Res. Commun. 46 (1972) 597-604
7. Berger I., Tereshko V., Ikeda H., Marquez V.E., and Egli M. Crystal structures of B-DNA with incorporated 2′-deoxy-2′-fluoro-arabino-furanosyl thymines: implications of conformational preorganization for duplex stability. Nucleic Acids Res. 26 (1998) 2473-2480
8. Bjelland S., Bjoras M., and Seeberg E. Excision of 3-methylguanine from alkylated DNA by 3-methyladenine DNA glycosylase I of Escherichia coli. Nucleic Acids Res. 21 (1993) 2045-2049
9. Bjelland S., Birkeland N.K., Benneche T., Volden G., and Seeberg E. DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the AlkA enzyme in Escherichia coli. J. Biol. Chem. 269 (1994) 30489-30495
10. 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
11. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
12. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
13. Corfield P.W., Hunter W.N., Brown T., Robinson P., and Kennard O. Inosine.adenine base pairs in a B-DNA duplex. Nucleic Acids Res. 15 (1987) 7935-7949
14. 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
15. Cote M.L., and Georgiadis M.M. Structure of a pseudo-16-mer DNA with stacked guanines and two G-A mispairs complexed with the N-terminal fragment of Moloney murine leukemia virus reverse transcriptase. Acta Crystallogr. D Biol. Crystallogr. 57 (2001) 1238-1250
16. Cote M.L., Yohannan S.J., and Georgiadis M.M. Use of an N-terminal fragment from moloney murine leukemia virus reverse transcriptase to facilitate crystallization and analysis of a pseudo-16-mer DNA molecule containing G-A mispairs. Acta Crystallogr. D Biol. Crystallogr. 56 (2000) 1120-1131
17. Cruse W.B., Aymani J., Kennard O., Brown T., Jack A.G., and Leonard G.A. Refined crystal structure of an octanucleotide duplex with I.T. mismatched base pairs. Nucleic Acids Res. 17 (1989) 55-72
18. DeLano Scientific LLC (2008). PyMOL (http://www.pymol.org).
19. Doherty A.J., Serpell L.C., and Ponting C.P. The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res. 24 (1996) 2488-2497
20. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
21. Engelward B.P., Allan J.M., Dreslin A.J., Kelly J.D., Wu M.M., Gold B., and Samson L.D. A chemical and genetic approach together define the biological consequences of 3-methyladenine lesions in the Mamm. Genome. J. Biol. Chem. 273 (1998) 5412-5418
22. Ferre-D'Amare A.R., and Doudna J.A. Crystallization and structure determination of a hepatitis delta virus ribozyme: use of the RNA-binding protein U1A as a crystallization module. J. Mol. Biol. 295 (2000) 541-556
23. Friedberg E.C., Walker G.C., and Siede W. DNA Repair and Mutagenesis (1995), American Society for Microbiology, Washington, D.C.
24. 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
25. Fromme J.C., and Verdine G.L. DNA lesion recognition by the bacterial repair enzyme MutM. J. Biol. Chem. 278 (2003) 51543-51548
26. 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
27. 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
28. 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
29. Goodwin K.D., Long E.C., and Georgiadis M.M. A host-guest approach for determining drug-DNA interactions: an example using netropsin. Nucleic Acids Res. 33 (2005) 4106-4116
30. Guan Y., Manuel R.C., Arvai A.S., Parikh S.S., Mol C.D., Miller J.H., Lloyd 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
31. Guengerich F.P., Crawford Jr. W.M., and Watanabe P.G. Activation of vinyl chloride to covalently bound metabolites: roles of 2-chloroethylene oxide and 2-chloroacetaldehyde. Biochemistry 18 (1979) 5177-5182
32. 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
33. Iwai S., Maeda M., Shirai M., Shimada Y., Osafune T., Murata T., and Ohtsuka E. Reaction mechanism of T4 endonuclease V determined by analysis using modified oligonucleotide duplexes. Biochemistry 34 (1995) 4601-4609
34. Jelinsky S.A., and Samson L.D. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Natl. Acad. Sci. USA 96 (1999) 1486-1491
35. Kouchakdjian M., Eisenberg M., Yarema K., Basu A., Essigmann J., and Patel D.J. NMR studies of the exocyclic 1,N6-ethenodeoxyadenosine adduct (ε dA) opposite thymidine in a DNA duplex. Nonplanar alignment of epsilon dA(anti) and dT(anti) at the lesion site. Biochemistry 30 (1991) 1820-1828
36. Kusmierek J.T., and Singer B. Chloroacetaldehyde-treated ribo- and deoxyribopolynucleotides. 1. Reaction products. Biochemistry 21 (1982) 5717-5722
37. Labahn J., Scharer O.D., Long A., Ezaz-Nikpay K., Verdine G.L., and Ellenberger T.E. Structural basis for the excision repair of alkylation-damaged DNA. Cell 86 (1996) 321-329
38. Leonard G.A., McAuley-Hecht K.E., Gibson N.J., Brown T., Watson W.P., and Hunter W.N. Guanine-1,N6-ethenoadenine base pairs in the crystal structure of d(CGCGAATT(ε dA)GCG). Biochemistry 33 (1994) 4755-4761
39. Leonard N.J. Etheno-substituted nucleotides and coenzymes: fluorescence and biological activity. CRC Crit. Rev. Biochem. 15 (1984) 125-199
40. Lindahl T. Molecular biology: ensuring error-free DNA repair. Nature 427 (2004) 598
41. Lingaraju G.M., Sartori A.A., Kostrewa D., Prota A.E., Jiricny J., and Winkler F.K. A DNA glycosylase from Pyrobaculum aerophilum with an 8-oxoguanine binding mode and a noncanonical helix-hairpin-helix structure. Structure 13 (2005) 87-98
42. Lipscomb L.A., Peek M.E., Morningstar M.L., Verghis S.M., Miller E.M., Rich A., Essigmann J.M., and Williams L.D. X-ray structure of a DNA decamer containing 7,8-dihydro-8-oxoguanine. Proc. Natl. Acad. Sci. USA 92 (1995) 719-723
43. 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
44. McAuley-Hecht K.E., Leonard G.A., Gibson N.J., Thomson J.B., Watson W.P., Hunter W.N., and Brown T. Crystal structure of a DNA duplex containing 8-hydroxydeoxyguanine-adenine base pairs. Biochemistry 33 (1994) 10266-10270
45. Nash H.M., Bruner S.D., Scharer O.D., Kawate T., Addona T.A., Spooner E., Lane W.S., and Verdine G.L. Cloning of a yeast 8-oxoguanine DNA glycosylase reveals the existence of a base-excision DNA-repair protein superfamily. Curr. Biol. 6 (1996) 968-980
46. 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
47. O'Brien P.J., and Ellenberger T. The Escherichia coli 3-methyladenine DNA glycosylase AlkA has a remarkably versatile active site. J. Biol. Chem. 279 (2004) 26876-26884
48. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallgr. A 276 (1997) 307-326
49. Radom C.T., Banerjee A., and Verdine G.L. Structural characterization of human 8-oxoguanine DNA glycosylase variants bearing active site mutations. J. Biol. Chem. 282 (2007) 9182-9194
50. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr. D Biol. Crystallogr. 57 (2001) 1373-1382
51. Saparbaev M., and Laval J. Excision of hypoxanthine from DNA containing dIMP residues by the Escherichia coli, yeast, rat, and human alkylpurine DNA glycosylases. Proc. Natl. Acad. Sci. USA 91 (1994) 5873-5877
52. Saparbaev M., Kleibl K., and Laval J. Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1,N6-ethenoadenine when present in DNA. Nucleic Acids Res. 23 (1995) 3750-3755
53. Scharer O.D., and Verdine G.L. A designed inhibitor of base-excision DNA repair. J. Am. Chem. Soc. 117 (1995) 10781-10782
54. Scharer O.D., Kawate T., Gallinari P., Jiricny J., and Verdine G.L. Investigation of the mechanisms of DNA binding of the human G/T glycosylase using designed inhibitors. Proc. Natl. Acad. Sci. USA 94 (1997) 4878-4883
55. 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
56. Shibutani S., Takeshita M., and Grollman A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349 (1991) 431-434
57. Shigenaga M.K., Gimeno C.J., and Ames B.N. Urinary 8-hydroxy-2′-deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc. Natl. Acad. Sci. USA 86 (1989) 9697-9701
58. Singer B., and Kusmierek J.T. Chemical mutagenesis. Annu. Rev. Biochem. 51 (1982) 655-693
59. Singer B., and Spengler S.J. Replication and transcription of polynucleotides containing ethenocytosine, ethenoadenine and their hydrated intermediates. IARC Sci. Publ. (1986) 359-371
60. Singer B., Abbott L.G., and Spengler S.J. Assessment of mutagenic efficiency of two carcinogen-modified nucleosides, 1,N6-ethenodeoxyadenosine and O4-methyldeoxythymidine, using polymerases of varying fidelity. Carcinogenesis 5 (1984) 1165-1171
61. 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
62. Terato H., Masaoka A., Asagoshi K., Honsho A., Ohyama Y., Suzuki T., Yamada M., Makino K., Yamamoto K., and Ide H. Novel repair activities of AlkA (3-methyladenine DNA glycosylase II) and endonuclease VIII for xanthine and oxanine, guanine lesions induced by nitric oxide and nitrous acid. Nucleic Acids Res. 30 (2002) 4975-4984
63. Wibley J.E., Waters T.R., Haushalter K., Verdine G.L., and Pearl L.H. Structure and specificity of the vertebrate anti-mutator uracil-DNA glycosylase SMUG1. Mol. Cell 11 (2003) 1647-1659
64. Zharkov D.O., Gilboa R., Yagil I., Kycia J.H., Gerchman S.E., Shoham G., and Grollman A.P. Role for lysine 142 in the excision of adenine from A:G mispairs by MutY DNA glycosylase of Escherichia coli. Biochemistry 39 (2000) 14768-14778
65. 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