Substrate binding pocket residues of human alkyladenine-DNA glycosylase critical for methylating agent survival

DNA Repair

Volumn 7, Issue 10, 2008, Pages 1731-1745

  Chen, Cheng Yao ^a   Guo, Haiwei H ^a   Shah, Dharini ^b   Blank, A ^a   Samson, Leona D ^b   Loeb, Lawrence A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

3 Methyladenine; 7 Methylguanine; Alkylating agents; Base excision repair; Methyl lexitropsin; Random mutagenesis

Indexed keywords

3 METHYLADENINE; 7 METHYLGUANINE; ADENINE DERIVATIVE; ALKYLADENINE; AMINO ACID; DNA; DNA GLYCOSYLTRANSFERASE; HISTIDINE; HYPOXANTHINE; LEUCINE; LEXITROPSIN; MESYLIC ACID METHYL ESTER; MUTANT PROTEIN; OLIGONUCLEOTIDE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CYTOTOXICITY; DNA DAMAGE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; EXCISION REPAIR; EXPRESSION VECTOR; IN VIVO STUDY; METHYLATION; MUTAGENESIS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; CATALYTIC DOMAIN; DNA ADDUCTS; DNA GLYCOSYLASES; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; HUMANS; METHYL METHANESULFONATE; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTANT PROTEINS; MUTATION; NETROPSIN; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

ESCHERICHIA COLI;

EID: 52049117381     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.06.019     Document Type: Article

References (42)

1. Sedgwick B. Repairing DNA-methylation damage. Nat. Rev. Mol. Cell. Biol. 5 (2004) 148-157
2. Wyatt M.D., and Pittman D.L. Methylating agents and DNA repair responses: methylated bases and sources of strand breaks. Chem. Res. Toxicol. 19 (2006) 1580-1594
3. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis (2005), American Society for Microbiology, Washington, DC
4. Doublie S., Tabor S., Long A.M., Richardson C.C., and Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391 (1998) 251-258
5. Beard W.A., Osheroff W.P., Prasad R., Sawaya M.R., Jaju M., Wood T.G., Kraut J., Kunkel T.A., and Wilson S.H. Enzyme-DNA interactions required for efficient nucleotide incorporation and discrimination in human DNA polymerase beta. J. Biol. Chem. 271 (1996) 12141-12144
6. Samson L.D., Derfler B., Boosalis M., and Call K. Cloning and characterization of a 3-methyladenine DNA glycosylase cDNA from human cells whose gene maps to chromosome 16. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 9127-9131
7. Engelward B.P., Dreslin A., Christensen J., Huszar D., Kurahara C., and Samson L.D. Repair-deficient 3-methyladenine DNA glycosylase homozygous mutant mouse cells have increased sensitivity to alkylation-induced chromosome damage and cell killing. EMBO J. 15 (1996) 945-952
8. 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 mammalian genome. J. Biol. Chem. 273 (1998) 5412-5418
9. Scharer O.D., and Jiricny J. Recent progress in the biology, chemistry and structural biology of DNA glycosylases. Bioessays 23 (2001) 270-281
10. Hosfield D.J., Daniels D.S., Mol C.D., Putnam C.D., Parikh S.S., and Tainer J.A. DNA damage recognition and repair pathway coordination revealed by the structural biochemistry of DNA repair enzymes. Prog. Nucleic Acid Res. Mol. Biol. 68 (2001) 315-347
11. Glassner B.J., Rasmussen L.J., Najarian M.T., Posnick L.M., and Samson L.D. Generation of a strong mutator phenotype in yeast by imbalanced base excision repair. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 9997-10002
12. Posnick L.M., and Samson L.D. Imbalanced base excision repair increases spontaneous mutation and alkylation sensitivity in Escherichia coli. J. Bacteriol. 181 (1999) 6763-6771
13. Wyatt M.D., Allan J.M., Lau A.Y., Ellenberger T.E., and Samson L.D. 3-Methyladenine DNA glycosylases: structure, function, and biological importance. Bioessays 21 (1999) 668-676
14. Wuenschell G.E., O'Connor T.R., and Termini J. Stability, miscoding potential, and repair of 2′-deoxyxanthosine in DNA: implications for nitric oxide-induced mutagenesis. Biochemistry 42 (2003) 3608-3616
15. Hitchcock T.M., Dong L., Connor E.E., Meira L.B., Samson L.D., Wyatt M.D., and Cao W. Oxanine DNA glycosylase activity from Mammalian alkyladenine glycosylase. J. Biol. Chem. 279 (2004) 38177-38183
16. Bessho T., Roy R., Yamamoto K., Kasai H., Nishimura S., Tano K., and Mitra S. Repair of 8-hydroxyguanine in DNA by mammalian N-methylpurine-DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 8901-8904
17. 6-ethenoadenine is preferred over 3-methyladenine as substrate by a cloned human N-methylpurine-DNA glycosylase (3-methyladenine-DNA glycosylase). Biochemistry 33 (1994) 1624-1628
18. Saparbaev M., Langouet S., Privezentzev C.V., Guengerich F.P., Cai H., Elder R.H., and Laval J. 1,N(2)-ethenoguanine, a mutagenic DNA adduct, is a primary substrate of Escherichia coli mismatch-specific uracil-DNA glycosylase and human alkylpurine-DNA-N-glycosylase. J. Biol. Chem. 277 (2002) 26987-26993
19. Berdal K.G., Johansen R.F., and Seeberg E. Release of normal bases from intact DNA by a native DNA repair enzyme. EMBO J. 17 (1998) 363-367
20. O'Brien P.J., and Ellenberger T. Dissecting the broad substrate specificity of human 3-methyladenine-DNA glycosylase. J. Biol. Chem. 279 (2004) 9750-9757
21. 6-ethenoadenine as preferred substrates. J. Biol. Chem. 279 (2004) 13601-13606
22. Lau A.Y., Scharer O.D., Samson L., Verdine G.L., and Ellenberger T. Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell 95 (1998) 249-258
23. Lau A.Y., Wyatt M.D., Glassner B.J., Samson L.D., and Ellenberger T. Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 13573-13578
24. Guo H.H., Choe J., and Loeb L.A. Protein tolerance to random amino acid change. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 9205-9210
25. Connor E.E., and Wyatt M.D. Active-site clashes prevent the human 3-methyladenine DNA glycosylase from improperly removing bases. Chem. Biol. 9 (2002) 1033-1041
26. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
27. Samson L.D., and Linn S. DNA alkylation repair and the induction of cell death and sister chromatid exchange in human cells. Carcinogenesis 8 (1987) 227-230
28. Encell L.P., Landis D.M., and Loeb L.A. Improving enzymes for cancer gene therapy. Nat. Biotechnol. 17 (1999) 143-147
29. 3-methyladenine. J. Cell. Biochem. 91 (2004) 250-257
30. Encell L., Shuker D.E., Foiles P.G., and Gold B. The in vitro methylation of DNA by a minor groove binding methyl sulfonate ester. Chem. Res. Toxicol. 9 (1996) 563-567
31. Kelly J.D., Inga A., Chen F.X., Dande P., Shah D., Monti P., Aprile A., Burns P.A., Scott G., Abbondandolo A., Gold B., and Fronza G. Relationship between DNA methylation and mutational patterns induced by a sequence selective minor groove methylating agent. J. Biol. Chem. 274 (1999) 18327-18334
32. O'Connor T.R. Purification and characterization of human 3-methyladenine-DNA glycosylase. Nucleic Acids Res. 21 (1993) 5561-5569
33. Rinne M.L., He Y., Pachkowski B.F., Nakamura J., and Kelley M.R. N-Methylpurine DNA glycosylase overexpression increases alkylation sensitivity by rapidly removing non-toxic 7-methylguanine adducts. Nucleic Acids Res. 33 (2005) 2859-2867
34. Allinson S.L., Sleeth K.M., Matthewman G.E., and Dianov G.L. Orchestration of base excision repair by controlling the rates of enzymatic activities. DNA Repair (Amst.) 3 (2004) 23-31
35. Gallivan J.P., and Dougherty D.A. Cation-pi interactions in structural biology. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 9459-9464
36. Hu G., Gershon P.D., Hodel A.E., and Quiocho F.A. mRNA cap recognition: dominant role of enhanced stacking interactions between methylated bases and protein aromatic side chains. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 7149-7154
37. Eichman B.F., O'Rourke E.J., Radicella J.P., and Ellenberger T. Crystal structures of 3-methyladenine DNA glycosylase MagIII and the recognition of alkylated bases. EMBO J. 22 (2003) 4898-4909
38. Maher R.L., Vallur A.C., Feller J.A., and Bloom L.B. Slow base excision by human alkyladenine DNA glycosylase limits the rate of formation of AP sites and AP endonuclease 1 does not stimulate base excision. DNA Repair (Amst.) 6 (2007) 71-81
39. Fishel M.L., Seo Y.R., Smith M.L., and Kelley M.R. Imbalancing the DNA base excision repair pathway in the mitochondria; targeting and overexpressing N-methylpurine DNA glycosylase in mitochondria leads to enhanced cell killing. Cancer Res. 63 (2003) 608-615
40. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N., and Bourne P.E. The Protein Data Bank. Nucleic Acids Res. 28 (2000) 235-242
41. Yang Y., Sass L.E., Du C., Hsieh P., and Erie D.A. Determination of protein-DNA binding constants and specificities from statistical analyses of single molecules: MutS-DNA interactions. Nucleic Acids Res. 33 (2005) 4322-4334
42. O'Brien P.J., and Ellenberger T. Human alkyladenine DNA glycosylase uses acid-base catalysis for selective excision of damaged purines. Biochemistry 42 (2003) 12418-12429