The DNA glycosylase AlkD uses a non-base-flipping mechanism to excise bulky lesions

Nature

Volumn 527, Issue 7577, 2015, Pages 254-258

  Mullins, Elwood A ^a   Shi, Rongxin ^a   Parsons, Zachary D ^a   Yuen, Philip K ^b   David, Sheila S ^b   Igarashi, Yasuhiro ^c   Eichman, Brandt F ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c TOYAMA PREFECTURAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFUNGAL AGENT; DNA GLYCOSYLASE ALKD; DNA GLYCOSYLTRANSFERASE; UNCLASSIFIED DRUG; YATAKEMYCIN; DNA ADDUCT; INDOLE DERIVATIVE; PYRROLE DERIVATIVE;

ANTIMICROBIAL ACTIVITY; BACTERIUM; CATALYSIS; DNA; DRUG; ENZYME ACTIVITY; LESION;

ARTICLE; BACILLUS CEREUS; CALCULATION; CATALYSIS; CRYSTALLOGRAPHY; DRUG MECHANISM; EXCISION; EXCISION REPAIR; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; BASE PAIRING; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DNA ADDUCT; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVE SITE; ENZYMOLOGY; METABOLISM; X RAY CRYSTALLOGRAPHY;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

BACILLUS CEREUS; BASE PAIRING; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA ADDUCTS; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; INDOLES; MODELS, MOLECULAR; PYRROLES;

EID: 84946917208     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature15728     Document Type: Article

References (56)

1. Fromme, J. C. & Verdine, G. L. Base excision repair. Adv. Protein Chem. 69, 1-41 (2004).
2. Hitomi, K., Iwai, S. & Tainer, J. A. The intricate structural chemistry of base excision repair machinery: implications for DNA damage recognition, removal, and repair. DNA Repair (Amst.) 6, 410-428 (2007).
3. Slupphaug, G. et al. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 384, 87-92 (1996).
4. Stivers, J. T. Site-specific DNA damage recognition by enzyme-induced base flipping. Prog. Nucleic Acid Res. Mol. Biol. 77, 37-65 (2004).
5. Brooks, S. C., Adhikary, S., Rubinson, E. H. & Eichman, B. F. Recent advances in the structural mechanisms of DNA glycosylases. Biochim. Biophys. Acta 1834, 247-271 (2013).
6. Igarashi, Y. et al. Yatakemycin, a novel antifungal antibiotic produced by Streptomyces sp. TP-A0356. J. Antibiot. (Tokyo) 56, 107-113 (2003).
7. Alberts, S. R., Suman, V. J., Pitot, H. C., Camoriano, J. K. & Rubin, J. Use of KW-2189, a DNA minor groove-binding agent, in patients with hepatocellular carcinoma: a north central cancer treatment group (NCCTG) phase II clinical trial. J. Gastrointest. Cancer 38, 10-14 (2007).
8. Friedberg, E. C. et al. DNA Repair and Mutagenesis 2nd edn (ASM Press, 2006).
9. Larson, K., Sahm, J., Shenkar, R. & Strauss, B. Methylation-induced blocks to in vitro DNA replication. Mutat. Res. 150, 77-84 (1985).
10. Plosky, B. S. et al. Eukaryotic Y-family polymerases bypass a 3-methyl-2′-deoxyadenosine analog in vitro and methyl methanesulfonate-induced DNA damage in vivo. Nucleic Acids Res. 36, 2152-2162 (2008).
11. Drohat, A. C. & Maiti, A. Mechanisms for enzymatic cleavage of the N-glycosidic bond in DNA. Org. Biomol. Chem. 12, 8367-8378 (2014).
12. Stivers, J. T. & Jiang, Y. L. A mechanistic perspective on the chemistry of DNA repair glycosylases. Chem. Rev. 103, 2729-2760 (2003).
13. Hendershot, J. M. & O'Brien, P. J. Critical role of DNA intercalation in enzyme-catalyzed nucleotide flipping. Nucleic Acids Res. 42, 12681-12690 (2014).
14. Alseth, I. et al. A new protein superfamily includes two novel 3-methyladenine DNA glycosylases from Bacillus cereus, AlkC and AlkD. Mol. Microbiol. 59, 1602-1609 (2006).
15. Rubinson, E. H., Metz, A. H., O'Quin, J. & Eichman, B. F. A new protein architecture for processing alkylation damaged DNA: the crystal structure of DNA glycosylase AlkD. J. Mol. Biol. 381, 13-23 (2008).
16. Rubinson, E. H., Gowda, A. S., Spratt, T. E., Gold, B. & Eichman, B. F. An unprecedented nucleic acid capture mechanism for excision of DNA damage. Nature 468, 406-411 (2010).
17. Dalhus, B. et al. Structural insight into repair of alkylated DNA by a new superfamily of DNA glycosylases comprising HEAT-like repeats. Nucleic Acids Res. 35, 2451-2459 (2007).
18. Mullins, E. A., Rubinson, E. H. & Eichman, B. F. The substrate binding interface of alkylpurine DNA glycosylase AlkD. DNA Repair (Amst.) 13, 50-54 (2014).
19. Mullins, E. A. et al. An HPLC-tandem mass spectrometry method for simultaneous detection of alkylated base excision repair products. Methods 64, 59-66 (2013).
20. Plevin, M. J., Bryce, D. L. & Boisbouvier, J. Direct detection of CH/π interactions in proteins. Nature Chem. 2, 466-471 (2010).
21. Yang, W. Poor base stacking at DNA lesions may initiate recognition by many repair proteins. DNA Repair (Amst.) 5, 654-666 (2006).
22. Brandl, M., Weiss, M. S., Jabs, A., Suhnel, J. & Hilgenfeld, R. C-H⋯π-interactions in proteins. J. Mol. Biol. 307, 357-377 (2001).
23. Wilson, K. A., Kellie, J. L. & Wetmore, S. D. DNA-protein π-interactions in nature: abundance, structure, composition and strength of contacts between aromatic amino acids and DNA nucleobases or deoxyribose sugar. Nucleic Acids Res. 42, 6726-6741 (2014).
24. Metz, A. H., Hollis, T. & Eichman, B. F. DNA damage recognition and repair by 3-methyladenine DNA glycosylase I (TAG). EMBO J. 26, 2411-2420 (2007).
25. Wilkinson, O. J. et al. Alkyltransferase-like protein (Atl1) distinguishes alkylated guanines for DNA repair using cation-π interactions. Proc. Natl Acad. Sci. USA 109, 18755-18760 (2012).
26. Tubbs, J. L. et al. Flipping of alkylated DNA damage bridges base and nucleotide excision repair. Nature 459, 808-813 (2009).
27. Xu, H. et al. Self-resistance to an antitumor antibiotic: a DNA glycosylase triggers the base-excision repair system in yatakemycin biosynthesis. Angew. Chem. Int. Ed. Engl. 51, 10532-10536 (2012).
28. Qi, Y. et al. Encounter and extrusion of an intrahelical lesion by a DNA repair enzyme. Nature 462, 762-766 (2009).
29. Imamura, K., Averill, A., Wallace, S. S. & Doublie, S. Structural characterization of viral ortholog of human DNA glycosylase NEIL1 bound to thymine glycol or 5-hydroxyuracil-containing DNA. J. Biol. Chem. 287, 4288-4298 (2012).
30. Adhikary, S. & Eichman, B. F. Analysis of substrate specificity of Schizosaccharomyces pombe Mag1 alkylpurine DNA glycosylase. EMBO Rep. 12, 1286-1292 (2011).
31. Chu, A. M., Fettinger, J. C. & David, S. S. Profiling base excision repair glycosylases with synthesized transition state analogs. Bioorg. Med. Chem. Lett. 21, 4969-4972 (2011).
32. O'Brien, P. J. & Ellenberger, T. Human alkyladenine DNA glycosylase uses acid-base catalysis for selective excision of damaged purines. Biochemistry 42, 12418-12429 (2003).
33. Bjelland, S., Birkeland, N. K., Benneche, T., Volden, G. & 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, 30489-30495 (1994).
34. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data. Methods Enzymol. 276, 307-326 (1997).
35. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
36. Emsley, P., Lohkamp, B., Scott, W. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
37. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
38. Davis, I. W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383 (2007).
39. Ho, B. K. & Gruswitz, F. HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8, 49 (2008).
40. Mike, L. A. et al. Two-component system cross-regulation integrates Bacillus anthracis response to heme and cell envelope stress. PLoS Pathog. 10, e1004044 (2014).
41. Sterne, M. Avirulent anthrax vaccine. Onderstepoort J. Vet. Sci. Anim. Ind. 21, 41-43 (1946).
42. Stauff, D. L. & Skaar, E. P. Bacillus anthracis HssRS signalling to HrtAB regulates haem resistance during infection. Mol. Microbiol. 72, 763-778 (2009).
43. a calculations: are we there yet? Theor. Chem. Acc. 125, 3-21 (2010).
44. Kapinos, L. E., Operschall, B. P., Larsen, E. & Sigel, H. Understanding the acid-base properties of adenosine: the intrinsic basicities of N1, N3 and N7. Chemistry 17, 8156-8164 (2011).
45. Zhao, Y. & Truhlar, D. G. The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theor. Chem. Acc. 120, 215-241 (2008).
46. Marenich, A. V., Cramer, C. J. & Truhlar, D. G. Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J. Phys. Chem. B 113, 6378-6396 (2009).
47. Dinner, A. R., Blackburn, G. M. & Karplus, M. Uracil-DNA glycosylase acts by substrate autocatalysis. Nature 413, 752-755 (2001).
48. Boys, S. F. & Bernardi, F. The calculation of small molecular interactions by the differences of separate total energies. Some procedures with reduced errors. Mol. Phys. 19, 553-566 (1970).
49. Shibasaki, K., Fujii, A., Mikami, N. & Tsuzuki, S. Magnitude of the CH/π interaction in the gas phase: experimental and theoretical determination of the accurate interaction energy in benzene-methane. J. Phys. Chem. A 110, 4397-4404 (2006).
50. δ+⋯X. Complexes of quaternary ions with n- and π-donors. J. Am. Chem. Soc. 107, 469-474 (1985).
51. Osborne, M. R. & Phillips, D. H. Preparation of a methylated DNA standard, and its stability on storage. Chem. Res. Toxicol. 13, 257-261 (2000).
52. Singh, U. C. & Kollman, P. A. An approach to computing electrostatic charges for molecules. J. Comput. Chem. 5, 129-145 (1984).
53. Besler, B. H., Merz, K. M. & Kollman, P. A. Atomic charges derived from semiempirical methods. J. Comput. Chem. 11, 431-439 (1990).
54. Ramstein, J. & Lavery, R. Energetic coupling between DNA bending and base pair opening. Proc. Natl Acad. Sci. USA 85, 7231-7235 (1988).
55. Adhikary, S., Cato, M. C., McGary, K. L., Rokas, A. & Eichman, B. F. Non-productive DNA damage binding by DNA glycosylase-like protein Mag2 from Schizosaccharomyces pombe. DNA Repair (Amst.) 12, 196-204 (2013).
56. Dalhus, B. et al. Sculpting of DNA at abasic sites by DNA glycosylase homolog Mag2. Structure 21, 154-166 (2013).