Step-by-step mechanism of DNA damage recognition by human 8-oxoguanine DNA glycosylase

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 1, 2014, Pages 387-395

  Kuznetsova, Alexandra A ^a,b   Kuznetsov, Nikita A ^a,b   Ishchenko, Alexander A ^a,c   Saparbaev, Murat K ^c   Fedorova, Olga S ^a,b  

^a INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

^b NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

^c INSTITUT GUSTAVE ROUSSY   (France)

Author keywords

Base excision repair; Conformational dynamics; DNA glycosylase; Enzyme kinetics; Human 8 oxoguanine DNA glycosylase

Indexed keywords

2 AMINOPURINE; 8 HYDROXYGUANINE; 8 HYDROXYGUANINE DNA GLYCOSYLASE; DNA; DNA BASE; DNA GLYCOSYLTRANSFERASE; DOUBLE STRANDED DNA; GUANINE; HISTIDINE; LYSINE; TRYPTOPHAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME MECHANISM; FLUORESCENCE ANALYSIS; HUMAN; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; MUTANT; PRIORITY JOURNAL; PROTEIN CONFORMATION; STEADY STATE; WILD TYPE;

(3-HYDROXYTETRAHYDROFURAN-2-YL)METHYL PHOSPHATE; 2-AMINOPURINE; 2-APU; 7,8-DIHYDRO-8-OXOGUANINE; BASE EXCISION REPAIR; BER; CONFORMATIONAL DYNAMICS; DNA GLYCOSYLASE; ENZYME KINETICS; HUMAN 8-OXOGUANINE DNA GLYCOSYLASE; ODN; OLIGODEOXYRIBONUCLEOTIDE; OXOG; THF;

BINDING SITES; CATALYSIS; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; GUANINE; HUMANS; KINETICS; MOLECULAR CONFORMATION; MUTANT PROTEINS; MUTATION; SPECTROMETRY, FLUORESCENCE;

EID: 84885541289     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.09.035     Document Type: Article

References (37)

1. S.S. Wallace Biological consequences of free radical-damaged DNA bases Free Radic. Biol. Med. 33 2002 1 14 (Pubitemid 34681001)
2. M.D. Evans, M. Dizdaroglu, and M.S. Cooke Oxidative DNA damage and disease: induction, repair and significance Mutat. Res. 567 2004 1 61 (Pubitemid 39162992)
3. T.A. Rosenquist, D.O. Zharkov, and A.P. Grollman Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase Proc. Natl. Acad. Sci. U. S. A. 94 1997 7429 7434 (Pubitemid 27345332)
4. D.O. Zharkov, T.A. Rosenquist, S.E. Gerchman, and A.P. Grollman Substrate specificity and reaction mechanism of murine 8-oxoguanine-DNA glycosylase J. Biol. Chem. 275 2000 28607 28617
5. P.A. van der Kemp, D. Thomas, R. Barbey, R. de Oliveira, and S. Boiteux Cloning and expression in Escherichia coli of the OGG1 gene of Saccharomyces cerevisiae, which codes for a DNA glycosylase that excises 7,8-dihydro-8- oxoguanine and 2,6-diamino-4-hydroxy-5-N-methylformamidopyrimidine Proc. Natl. Acad. Sci. U. S. A. 93 1996 5197 5202
6. J.P. Radicella, C. Dherin, C. Desmaze, M.S. Fox, and S. Boiteux Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae Proc. Natl. Acad. Sci. U. S. A. 94 1997 8010 8015 (Pubitemid 27343767)
7. M. Bjoras, L. Luna, B. Johnsen, E. Hoff, T. Haug, T. Rognes, and E. Seeberg Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites EMBO J. 16 1997 6314 6322 (Pubitemid 27458351)
8. S. Shibutani, M. Takeshita, and A.P. Grollman Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG Nature 349 1991 431 434 (Pubitemid 21926107)
9. K. Asagoshi, T. Yamada, H. Terato, Y. Ohyama, Y. Monden, T. Arai, S. Nishimura, H. Aburatani, T. Lindahli, and H. Ide Distinct repair activities of human 7,8-dihydro-8-oxoguanine DNA glycosylase and formamidopyrimidine DNA glycosylase for formamidopyrimidine and 7,8-dihydro-8-oxoguanine J. Biol. Chem. 275 2000 4956 4964 (Pubitemid 30108891)
10. P.M. Girard, N. Guibourt, and S. Boiteux The Ogg1 protein of Saccharomyces cerevisiae: a 7,8-dihydro-8-oxoguanine DNA glycosylase/AP lyase whose lysine 241 is a critical residue for catalytic activity Nucleic Acids Res. 25 1997 3404 3411
11. H.M. Nash, R. Lu, W.S. Lane, and G.L. Verdine The critical active-site amine of the human 8-oxoguanine DNA glycosylase, hOgg1: direct identification, ablation and chemical reconstitution Chem. Biol. 4 1997 693 702 (Pubitemid 27426627)
12. M.M. Thayer, H. Ahern, D. Xing, R.P. Cunningham, and J.A. Tainer Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure EMBO J. 14 1995 4108 4120
13. J. Labahn, O.D. Schärer, A. Long, K. Ezaz-Nikpay, G.L. Verdine, and T.E. Ellenberger Structural basis for the excision repair of alkylation-damaged DNA Cell 86 1996 321 329 (Pubitemid 26286114)
14. Y. Guan, R.C. Manuel, A.S. Arvai, S.S. Parikh, C.D. Mol, J.H. Miller, R.S. Lloyd, and J.A. Tainer MutY catalytic core, mutant and bound adenine structures define specificity for DNA repair enzyme superfamily Nat. Struct. Biol. 5 1998 1058 1064 (Pubitemid 28546269)
15. D.P. Norman, S.J. Chung, and G.L. Verdine Structural and biochemical exploration of a critical amino acid in human 8-oxoguanine glycosylase Biochemistry 42 2003 1564 1572 (Pubitemid 36205963)
16. B. Dalhus, M. Forsbring, I.H. Helle, E.S. Vik, R.J. Forstrom, P.H. Backe, I. Alseth, and M. Bjoras Separation-of-function mutants unravel the dual-reaction mode of human 8-oxoguanine DNA glycosylase Structure 19 2011 117 127
17. S.D. Bruner, D.P. Norman, and G.L. Verdine Structural basis for recognition and repair of the endogenous mutagen 8-oxoguanine in DNA Nature 403 2000 859 866 (Pubitemid 30130980)
18. M. Bjoras, E. Seeberg, L. Luna, L.H. Pearl, and T.E. Barrett Reciprocal "flipping" underlies substrate recognition and catalytic activation by the human 8-oxo-guanine DNA glycosylase J. Mol. Biol. 317 2002 171 177 (Pubitemid 34722185)
19. A. Banerjee, W. Yang, M. Karplus, and G.L. Verdine Structure of a repair enzyme interrogating undamaged DNA elucidates recognition of damaged DNA Nature 434 2005 612 618 (Pubitemid 40488548)
20. C.T. Radom, A. Banerjee, and G.L. Verdine Structural characterization of human 8-oxoguanine DNA glycosylase variants bearing active site mutations J. Biol. Chem. 282 2007 9182 9194
21. C.M. Crenshaw, K. Nam, K. Oo, P.S. Kutchukian, B.R. Bowman, M. Karplus, and G.L. Verdine Enforced presentation of an extrahelical guanine to the lesion recognition pocket of human 8-oxoguanine glycosylase, hOGG1 J. Biol. Chem. 287 2012 24916 24928
22. N.A. Kuznetsov, V.V. Koval, D.O. Zharkov, G.A. Nevinsky, K.T. Douglas, and O.S. Fedorova Kinetics of substrate recognition and cleavage by human 8-oxoguanine-DNA glycosylase Nucleic Acids Res. 33 2005 3919 3931 (Pubitemid 41418560)
23. N.A. Kuznetsov, V.V. Koval, G.A. Nevinsky, K.T. Douglas, D.O. Zharkov, and O.S. Fedorova Kinetic conformational analysis of human 8-oxoguanine-DNA glycosylase J. Biol. Chem. 282 2007 1029 1038 (Pubitemid 47076516)
24. K.A. Johnson Advances in transient-state kinetics Curr. Opin. Biotechnol. 9 1998 87 89 (Pubitemid 28098320)
25. P. Kuzmic Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase Anal. Biochem. 237 1996 260 273 (Pubitemid 26177089)
26. P.A. van der Kemp, J.B. Charbonnier, M. Audebert, and S. Boiteux Catalytic and DNA-binding properties of the human Ogg1 DNA N-glycosylase/AP lyase: biochemical exploration of H270, Q315 and F319, three amino acids of the 8-oxoguanine-binding pocket Nucleic Acids Res. 32 2004 570 578 (Pubitemid 38263048)
27. N. Guibourt, B. Castaing, P.A. Van Der Kemp, and S. Boiteux Catalytic and DNA binding properties of the ogg1 protein of Saccharomyces cerevisiae: comparison between the wild type and the K241R and K241Q active-site mutant proteins Biochemistry 39 2000 1716 1724 (Pubitemid 30108962)
28. D.P. Norman, S.D. Bruner, and G.L. Verdine Coupling of substrate recognition and catalysis by a human base-excision DNA repair protein J. Am. Chem. Soc. 123 2001 359 360 (Pubitemid 32062186)
29. M. Audebert, J.P. Radicella, and M. Dizdaroglu Effect of single mutations in the OGG1 gene found in human tumors on the substrate specificity of the Ogg1 protein Nucleic Acids Res. 28 2000 2672 2678 (Pubitemid 30488010)
30. F. Faucher, S.S. Wallace, and S. Doublie Structural basis for the lack of opposite base specificity of Clostridium acetobutylicum 8-oxoguanine DNA glycosylase DNA Repair (Amst) 8 2009 1283 1289
31. V.V. Koval, N.A. Kuznetsov, A.A. Ishchenko, M.K. Saparbaev, and O.S. Fedorova Real-time studies of conformational dynamics of the repair enzyme E. coli formamidopyrimidine-DNA glycosylase and its DNA complexes during catalytic cycle Mutat. Res. 685 2010 3 10
32. A.R. Dunn, N.M. Kad, S.R. Nelson, D.M. Warshaw, and S.S. Wallace Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA Nucleic Acids Res. 39 2011 7487 7498
33. M. Rogacheva, A. Ishchenko, M. Saparbaev, S. Kuznetsova, and V. Ogryzko High resolution characterization of formamidopyrimidine-DNA glycosylase interaction with its substrate by chemical cross-linking and mass spectrometry using substrate analogs J. Biol. Chem. 281 2006 32353 32365 (Pubitemid 46036790)
34. S.D. Williams, and S.S. David Formation of a Schiff base intermediate is not required for the adenine glycosylase activity of Escherichia coli MutY Biochemistry 38 1999 15417 15424 (Pubitemid 129503582)
35. D.O. Zharkov, R. Gilboa, I. Yagil, J.H. Kycia, S.E. Gerchman, G. Shoham, and A.P. Grollman 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
36. T. Hollis, Y. Ichikawa, and T. Ellenberger 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 (Pubitemid 30093749)
37. S. Lee, G.L. Verdine, Atomic substitution reveals the structural basis for substrate adenine recognition and removal by adenine DNA glycosylase, Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 1849718502.