Crystal structures of 3-methyladenine DNA glycosylase MagIII and the recognition of alkylated bases

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 4898-4909

  Eichman, Brandt F ^a   O'Rourke, Eyleen J ^a,b   Radicella, J Pablo ^b   Ellenberger, Tom ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

3 methyladenine; Base excision; DNA repair; Glycosylase; Helix hairpin helix

Indexed keywords

1,N6 ETHENOADENINE; 3 METHYLADENINE; 3,9 DIMETHYLADENINE; 7 METHYLGUANINE; ADENINE DERIVATIVE; DNA; DNA GLYCOSYLTRANSFERASE; HHH GLYCOSYLASE; NUCLEIC ACID BASE; PROTEIN MAGLLL; UNCLASSIFIED DRUG;

ALKYLATION; ARTICLE; BINDING AFFINITY; CHEMICAL MODIFICATION; COMPLEX FORMATION; CRYSTAL STRUCTURE; DNA BINDING; DNA DAMAGE; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; EXCISION; EXCISION REPAIR; HELICOBACTER PYLORI; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN FAMILY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; DNA REPAIR; MOLECULAR SEQUENCE DATA; N-GLYCOSYL HYDROLASES; PROTEIN STRUCTURE, TERTIARY;

HELICOBACTER; HELICOBACTER PYLORI;

EID: 0141754009     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg505     Document Type: Article

References (49)

1. Asaeda, A., Ide, H., Asagoshi, K., Matsuyama, S., Tano, K., Murakami, A., Takamori, Y. and Kubo, K. (2000) Substrate specificity of human methylpurine DNA N-glycosylase. Biochemistry, 39, 1959-1965.
2. Begley, T.J., Haas, B.J., Noel, J., Shekhtman, A., Williams, W.A. and Cunningham, R.P. (1999) A new member of the endonuclease III family of DNA repair enzymes that removes methylated purines from DNA. Curr. Biol., 9, 653-656.
3. Berdal, K.G., Johansen, R.F. and Seeberg, E. (1998) Release of normal bases from intact DNA by a native DNA repair enzyme. EMBO J., 17, 363-367.
4. Bjelland, S., Bjoras, M. and Seeberg, E. (1993) Excision of 3-methylguanine from alkylated DNA by 3-methyladenine DNA glycosylase I of Escherichia coli. Nucleic Acids Res., 21, 2045-2049.
5. Bjelland, S., Birkeland, N.K., Benneche, T., Volden, G. and Seeberg, E. (1994) DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the AlkA enzyme in Escherichia coli. J. Biol. Chem., 269, 30489-30495.
6. Bruner, S.D., Norman, D.P. and Verdine, G.L. (2000) Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA. Nature, 403, 859-866.
7. Brünger, A.T. (1992) Free R-Value-a Novel Statistical Quantity for Assessing the Accuracy of Crystal-Structures. Nature, 355, 472-475.
8. Bruns, C.M., Hubatsch, I., Ridderstrom, M., Mannervik, B. and Tainer, J.A. (1999) Human glutathione transferase A4-4 crystal structures and mutagenesis reveal the basis of high catalytic efficiency with toxic lipid peroxidation products. J. Mol. Biol., 288, 427-439.
9. Collaborative Computational Project (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallog., D50, 760-763.
10. Doherty, A.J., Serpell, L.C. and Ponting, C.P. (1996) The helix-hairpin-helix DNA-binding motif: a structural basis for non-sequence-specific recognition of DNA. Nucleic Acids Res., 24, 2488-2497.
11. Dougherty, D.A. (1996) Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr and Trp. Science, 271, 163-168.
12. Drohat, A.C., Kwon, K., Krosky, D.J. and Stivers, J.T. (2002) 3-Methyladenine DNA glycosylase I is an unexpected helix-hairpin-helix superfamily member. Nat. Struct. Biol., 9, 659-664.
13. Friedberg, E.C., Walker, G.C. and Siede, W. (1995) DNA Repair and Mutagenesis. ASM Press, Washington, DC.
14. Fujii, T., Itaya, T., Saito, T., Mohri, K., Kawanishi, M. and Nakasaka, T. (1989) Purines. XXXII. Synthesis and Ring Fission of 3,9-Dialkyladenines. Chem. Pharm. Bull., 37, 1504-1513.
15. Guan, Y., Manuel, R.C., Arvai, A.S., Parikh, S.S., Mol, C.D., Miller, J.H., Lloyd, S. and Tainer, J.A. (1998) MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily. Nat. Struct. Biol., 5, 1058-1064.
16. Hodel, A.E., Gershon, P.D., Shi, X., Wang, S.M. and Quiocho, F.A. (1997) Specific protein recognition of an mRNA cap through its alkylated base. Nat. Struct. Biol., 4, 350-354.
17. Hollis, T., Ichikawa, Y. and Ellenberger, T. (2000) DNA bending and a flip-out mechanism for base excision by the helix-hairpin-helix DNA glycosylase, Escherichia coli AlkA. EMBO J., 19, 758-766.
18. 7G mRNA cap. Biochemistry, 39, 13730-13736.
19. Hu, G., Gershon, P.D., Hodel, A.E. and Quiocho, F.A. (1999) mRNA cap recognition: dominant role of enhanced stacking interactions between methylated bases and protein aromatic side chains. Proc. Natl Acad. Sci. USA, 96, 7149-7154.
20. Ishida, T., Shibata, M., Fujii, K. and Inoue, M. (1983) Inter- and intramolecular stacking interaction between indole and adeninium rings. Biochemistry, 22, 3571-3581.
21. Ishida, T., Doi, M. and Inoue, M. (1988a) A selective recognition mode of a nucleic acid base by an aromatic amino acid: L-phenylalanine-7-methylguanosine 5′-monophosphate stacking interaction. Nucleic Acids Res., 16, 6175-6190.
22. Ishida, T., Doi, M., Ueda, H., Inoue, M. and Scheldrick, G.M. (1988b) Specific Ring Stacking Interaction on the Tryptophan 7-Methylguanine System: Comparative Crystallographic Studies of Indole-Derivatives 7-Methylguanine Base, Nucleoside and Nucleotide Complexes. J. Am. Chem. Soc., 110, 2286-2294.
23. Kuo, C.F., MeRee, D.E., Fisher, C.L., O'Handley, S.F., Cunningham, R.P. and Tainer, J.A. (1992) Atomic structure of the DNA repair [4Fe-4S] enzyme endonuclease III. Science, 258, 434-440.
24. Kwon, K., Cao, C. and Stivers, J.T. (2003) A novel zinc snap motif conveys structural stability to 3-methyladenine DNA glycosylase I. J. Biol. Chem., 278, 19442-19446.
25. Labahn, J., Schärer, O.D., Long, A., Ezaz-Nikpay, K., Verdine, G.L. and Ellenberger, T.E. (1996) Structural basis for the excision repair of alkylation-damaged DNA. Cell, 86, 321-329.
26. Lau, A.Y., Wyatt, M.D., Glassner, B.J., Samson, L.D. and Ellenberger, T. (2000) Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proc. Natl Acad. Sci. USA, 97, 13573-13578.
27. Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature, 362, 709-715.
28. Makino, K. and Ichikawa, Y. (1998) Synthesis of a 2-deoxy-ribose type 1-N-iminosugar. Tetrahedron Lett., 39, 8245-8248.
29. Marcotrigiano, J., Gingras, A.C., Sonenberg, N. and Burley, S.K. (1997) Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell, 89, 951-961.
30. 7GpppG cap analogue by the human nuclear cap-binding complex. EMBO J., 21, 5548-5557.
31. McCarthy, T.V., Karran, P. and Lindahl, T. (1984) Inducible repair of O-alkylated DNA pyrimidines in Escherichia coli. EMBO J., 3, 545-550.
32. McRee, D.E. (1999) XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol., 125, 156-165.
33. Mol, C.D., Arvai, A.S., Begley, T.J., Cunningham, R.P. and Tainer, J.A. (2002) Structure and activity of a thermostable thymine-DNA glycosylase: evidence for base twisting to remove mismatched normal DNA bases. J. Mol. Biol., 315, 373-384.
34. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of Macromolecular Structures by the Maximum-Likelihood Method. Acta Crystallog., D53, 240-255.
35. Nash, H.M., Bruner, S.D., Scharer, O.D., Kawate, T., Addona, T.A., Spooner, E., Lane, W.S. and Verdine, G.L. (1996) Cloning of a yeast 8-oxoguanine DNA glycosylase reveals the existence of a base-excision DNA-repair protein superfamily. Curr. Biol., 6, 968-980.
36. Nash, H.M., Lu, R., Lane, W.S. and Verdine, G.L. (1997) The critical active-site amine of the human 8-oxoguanine DNA glycosylase, hOgg1: direct identification, ablation and chemical reconstitution. Chem. Biol., 4, 693-702.
37. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
38. Norman, D.P., Chung, S.J. and Verdine, G.L. (2003) Structural and biochemical exploration of a critical amino acid in human 8-oxoguanine glycosylase. Biochemistry, 42, 1564-1572.
39. O'Rourke, E.J., Chevalier, C., Boiteux, S., Labigne, A., Ielpi, L. and Radicella, J.P. (2000) A novel 3-methyladenine DNA glycosylase from Helicobacter pylori defines a new class within the endonuclease III family of base excision repair glycosylases. J. Biol. Chem., 275, 20077-20083.
40. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
41. Roberts, R.J. and Cheng, X. (1998) Base flipping. Annu. Rev. Biochem., 67, 181-198.
42. 6-ethenoadenine when present in DNA. Nucleic Acids Res., 23, 3750-3755.
43. Schärer, O.D. and Jiricny, J. (2001) Recent progress in the biology, chemistry and structural biology of DNA glycosylases. BioEssays, 23, 270-281.
44. Schärer, O.D., Ortholand, J.-Y., Ganesan, A., Ezaz-Nikpay, K. and Verdine, G.L. (1995) Specific binding of the DNA repair enzyme AlkA to a pyrrolidine-based inhibitor. J. Am. Chem. Soc., 117, 6623-6624.
45. Terwilliger, T.C. (2000) Maximum likelihood density modification. Acta Crystallog., D56, 965-972.
46. Terwilliger, T.C. and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallog., D55, 849-861.
47. Thayer, M.M., Ahern, H., Xing, D., Cunningham, R.P. and Tainer, J.A. (1995) Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J., 14, 4108-4120.
48. Wu, P., Qiu, C., Sohail, A., Zhang, X., Bhagwat, A.S. and Cheng, X. (2003) Mismatch repair in methylated DNA. Structure and activity of the mismatch-specific thymine glycosylase domain of methyl-CpG-binding protein MBD4. J. Biol. Chem., 278, 5285-5291.
49. Yamagata, Y. et al. (1996) Three-dimensional structure of a DNA repair enzyme, 3-methyladenine DNA glycosylase II, from Escherichia coli. Cell, 86, 311-319.