The formation of catalytically competent enzyme–substrate complex is not a bottleneck in lesion excision by human alkyladenine DNA glycosylase

References

• Abner, C. W. , Lau, A. Y. , Ellenberger, T. , & Bloom, L. B. (2001). Base excision and DNA binding activities of human alkyladenine DNA glycosylase are sensitive to the base paired with a lesion. Journal of Biological Chemistry , 276 , 13379–13387.10.1074/jbc.M010641200
   PubMed Web of Science ®Google Scholar
• Adhikari, S. , Üren, A. , & Roy, S. (2009). Excised damaged base determines the turnover of human N-methylpurine-DNA glycosylase. DNA Repair , 8 , 1201–1206.10.1016/j.dnarep.2009.06.005
   PubMedGoogle Scholar
• Asaeda, A. , Ide, H. , Asagoshi, K. , Matsuyama, S. , Tano, K. , Murakami, A. , & Kubo, K. (2000). Substrate specificity of human methylpurine DNA N-glycosylase. Biochemistry , 39 , 1959–1965.10.1021/bi9917075
   PubMed Web of Science ®Google Scholar
• Baldwin, M. R. , & O’Brien, P. J. (2009). Human AP endonuclease 1 stimulates multiple-turnover base excision by alkyladenine DNA glycosylase. Biochemistry , 48 , 6022–6033.10.1021/bi900517y
   PubMed Web of Science ®Google Scholar
• Barnes, D. E. , & Lindahl, T. (2004). Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annual Review of Genetics , 38 , 445–476.10.1146/annurev.genet.38.072902.092448
   PubMed Web of Science ®Google Scholar
• Beranek, D. T. (1990). Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis , 231 , 11–30.10.1016/0027-5107(90)90173-2
   PubMed Web of Science ®Google Scholar
• Boelens, R. , Scheek, R. M. , Dijkstra, K. , & Kaptein, R. (1985). Sequential assignment of imino-proton and amino-proton resonances in H-1-NMR spectra of oligonucleotides by two-dimensional NMR-spectroscopy – Application to a Lac operator fragment. Journal of Magnetic Resonance , 62 , 378–386.
   Web of Science ®Google Scholar
• Carbonnaux, C. , Fazakerley, G. V. , & Sowers, L. C. (1990). An NMR structural study of deaminated base pairs in DNA. Nucleic Acids Research , 18 , 4075–4081.10.1093/nar/18.14.4075
   PubMed Web of Science ®Google Scholar
• David, R. L. (2005). CRC handbook of chemistry and physics . Boca Raton, FL: CRC Press.
   Google Scholar
• David, S. S. , & Williams, S. D. (1998). Chemistry of glycosylases and endonucleases involved in base-excision repair. Chemical Reviews , 98 , 1221–1262.10.1021/cr980321h
   PubMed Web of Science ®Google Scholar
• Dunlap, C. A. , & Tsai, M. D. (2002). Use of 2-aminopurine and tryptophan fluorescence as probes in kinetic analyses of DNA polymerase β. Biochemistry , 41 , 11226–11235.10.1021/bi025837g
   PubMed Web of Science ®Google Scholar
• Englander, S. W. , & Kallenbach, N. R. (1983). Hydrogen exchange and structural dynamics of proteins and nucleic acids. Quarterly Reviews of Biophysics , 16 , 521–655.10.1017/S0033583500005217
   PubMed Web of Science ®Google Scholar
• Fasman, G. D. (1975). Handbook of biochemistry and molecular biology ( 3 ed., Vol. 2). Cleveland, OH: CRC Press.
   Google Scholar
• Friedberg, E. C. , Walker, G. C. , Siede, W. , Wood, R. D. , Schultz, R. A. , & Ellenberger, T. (2006). DNA repair and mutagenesis . Washington, DC: ASM Press.
   Google Scholar
• Fromme, J. C. , Bruner, S. D. , Yang, W. , Karplus, M. , & Verdine, G. L. (2003). Product-assisted catalysis in base-excision DNA repair. Nature Structural Biology , 10 , 204–211.10.1038/nsb902
   PubMedGoogle Scholar
• Gill, S. C. , & von Hippel, P. H. (1989). Calculation of protein extinction coefficients from amino acid sequence data. Analytical Biochemistry , 182 , 319–326.10.1016/0003-2697(89)90602-7
   PubMed Web of Science ®Google Scholar
• Goddard, T. D. , & Kneller, D. G. (2008). SPARKY 3 . San Francisco: University of California.
   Google Scholar
• Gros, L. , Saparbaev, M. K. , & Laval, J. (2002). Enzymology of the repair of free radicals-induced DNA damage. Oncogene , 21 , 8905–8925.10.1038/sj.onc.1206005
   PubMed Web of Science ®Google Scholar
• Guéron, M. , & Leroy, J. L. (1995). Studies of base pair kinetics by NMR measurement of proton exchange. Methods in Enzymology , 261 , 383–413.10.1016/S0076-6879(95)61018-9
   PubMed Web of Science ®Google Scholar
• Hendershot, J. M. , & O’Brien, P. J. (2014). Critical role of DNA intercalation in enzyme-catalyzed nucleotide flipping. Nucleic Acids Research , 42 , 12681–12690.10.1093/nar/gku919
   PubMed Web of Science ®Google Scholar
• Hitchcock, T. M. , Dong, L. , Connor, E. E. , Meira, L. B. , Samson, L. D. , Wyatt, M. D. , & Cao, W. (2004). Oxanine DNA glycosylase activity from mammalian alkyladenine glycosylase. Journal of Biological Chemistry , 279 , 38177–38183.10.1074/jbc.M405882200
   PubMed Web of Science ®Google Scholar
• Hollis, T. , Lau, A. , & Ellenberger, T. (2000). Structural studies of human alkyladenine glycosylase and E. coli 3-methyladenine glycosylase. Mutation Research/DNA Repair , 460 , 201–210.10.1016/S0921-8777(00)00027-6
   Google Scholar
• Hwang, T. L. , & Shaka, A. J. (1995). Water suppression that works – Excitation sculpting using arbitrary wave-forms and pulsed-field gradients. Journal of Magnetic Resonance, Series A , 112 , 275–279.10.1006/jmra.1995.1047
   Google Scholar
• Jean, J. M. , & Hall, K. B. (2001). 2-Aminopurine fluorescence quenching and lifetimes: Role of base stacking. Proceedings of the National Academy of Sciences , 98 , 37–41.10.1073/pnas.98.1.37
   PubMed Web of Science ®Google Scholar
• Kaina, B. , Christmann, M. , Naumann, S. , & Roos, W. P. (2007). MGMT: Key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair , 6 , 1079–1099.10.1016/j.dnarep.2007.03.008
   PubMed Web of Science ®Google Scholar
• Kanazhevskaya, L. Y. , Koval, V. V. , Vorobjev, Y. N. , & Fedorova, O. S. (2012). Conformational dynamics of abasic DNA upon interactions with AP endonuclease 1 revealed by stopped-flow fluorescence analysis. Biochemistry , 51 , 1306–1321.10.1021/bi201444m
   PubMed Web of Science ®Google Scholar
• Kondo, N. , Takahashi, A. , Ono, K. , & Ohnishi, T. (2010). DNA damage induced by alkylating agents and repair pathways. Journal of Nucleic Acids , 2010 , 543531.
   PubMedGoogle Scholar
• Koval, V. V. , Kuznetsov, N. A. , Ishchenko, A. A. , Saparbaev, M. K. , & Fedorova, O. S. (2010). Real-time studies of conformational dynamics of the repair enzyme E. coli formamidopyrimidine-DNA glycosylase and its DNA complexes during catalytic cycle. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis , 685 , 3–10.10.1016/j.mrfmmm.2009.08.018
   PubMed Web of Science ®Google Scholar
• Koval, V. V. , Kuznetsov, N. A. , Zharkov, D. O. , Ishchenko, A. A. , Douglas, K. T. , Nevinsky, G. A. , & Fedorova, O. S. (2004). Pre-steady-state kinetics shows differences in processing of various DNA lesions by Escherichia coli formamidopyrimidine-DNA glycosylase. Nucleic Acids Research , 32 , 926–935.10.1093/nar/gkh237
   PubMed Web of Science ®Google Scholar
• Kuzmič, P. (1996). Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase. Analytical Biochemistry , 237 , 260–273.10.1006/abio.1996.0238
   PubMed Web of Science ®Google Scholar
• Kuznetsov, N. A. , Kladova, O. A. , Kuznetsova, A. A. , Ishchenko, A. A. , Saparbaev, M. K. , Zharkov, D. O. , & Fedorova, O. S. (2015). Conformational dynamics of DNA repair by Escherichia coli endonuclease III. Journal of Biological Chemistry , 290 , 14338–14349.10.1074/jbc.M114.621128
   PubMed Web of Science ®Google Scholar
• Kuznetsov, N. A. , Koval, V. V. , Nevinsky, G. A. , Douglas, K. T. , Zharkov, D. O. , & Fedorova, O. S. (2007). Kinetic conformational analysis of human 8-oxoguanine-DNA glycosylase. Journal of Biological Chemistry , 282 , 1029–1038.10.1074/jbc.M605788200
   PubMed Web of Science ®Google Scholar
• Kuznetsov, N. A. , Koval, V. V. , Zharkov, D. O. , Nevinsky, G. A. , Douglas, K. T. , & Fedorova, O. S. (2005). Kinetics of substrate recognition and cleavage by human 8-oxoguanine-DNA glycosylase. Nucleic Acids Research , 33 , 3919–3931.10.1093/nar/gki694
   PubMed Web of Science ®Google Scholar
• Kuznetsov, N. A. , Koval, V. V. , Zharkov, D. O. , Vorobjev, Y. N. , Nevinsky, G. A. , Douglas, K. T. , & Fedorova, O. S. (2007). Kinetic basis of lesion specificity and opposite-base specificity of Escherichia coli formamidopyrimidine-DNA glycosylase. Biochemistry , 46 , 424–435.10.1021/bi060787r
   PubMed Web of Science ®Google Scholar
• Kuznetsov, N. A. , Vorobjev, Y. N. , Krasnoperov, L. N. , & Fedorova, O. S. (2012). Thermodynamics of the multi-stage DNA lesion recognition and repair by formamidopyrimidine-DNA glycosylase using pyrrolocytosine fluorescence – Stopped-flow pre-steady-state kinetics. Nucleic Acids Research , 40 , 7384–7392.10.1093/nar/gks423
   PubMed Web of Science ®Google Scholar
• Kuznetsova, A. A. , Kuznetsov, N. A. , Ishchenko, A. A. , Saparbaev, M. K. , & Fedorova, O. S. (2014). Step-by-step mechanism of DNA damage recognition by human 8-oxoguanine DNA glycosylase. Biochimica et Biophysica Acta (BBA) – General Subjects , 1840 , 387–395.10.1016/j.bbagen.2013.09.035
   PubMed Web of Science ®Google Scholar
• Kuznetsova, A. A. , Kuznetsov, N. A. , Vorobjev, Y. N. , Barthes, N. P. , Michel, B. Y. , Burger, A. , & Fedorova, O. S. (2014). New environment-sensitive multichannel DNA fluorescent label for investigation of the protein–DNA interactions. PLoS ONE , 9 , e100007.10.1371/journal.pone.0100007
   PubMed Web of Science ®Google Scholar
• Lau, A. Y. , Schärer, O. D. , Samson, L. , Verdine, G. L. , & Ellenberger, T. (1998). Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA. Cell , 95 , 249–258.10.1016/S0092-8674(00)81755-9
   PubMed Web of Science ®Google Scholar
• Lau, A. Y. , Wyatt, M. D. , Glassner, B. J. , Samson, L. D. , & Ellenberger, T. (2000). Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, AAG. Proceedings of the National Academy of Sciences , 97 , 13573–13578.10.1073/pnas.97.25.13573
   PubMed Web of Science ®Google Scholar
• Lenz, S. A. , & Wetmore, S. D. (2016). Evaluating the substrate selectivity of alkyladenine DNA glycosylase: The synergistic interplay of active site flexibility and water reorganization. Biochemistry , 55 , 798–808.10.1021/acs.biochem.5b01179
   PubMed Web of Science ®Google Scholar
• Leonard, N. J. (1984). Etheno-substituted nucleotides and coenzymes: Fluorescence and biological activity. Critical Reviews in Biochemistry , 15 , 125–199.10.3109/10409238409102299
   PubMed Web of Science ®Google Scholar
• Moe, J. G. , & Russu, I. M. (1992). Kinetics and energetics of base-pair opening in 5’-D(Cgcgaattcgcg)-3’ and a substituted dodecamer containing G.T mismatches. Biochemistry , 31 , 8421–8428.10.1021/bi00151a005
   PubMed Web of Science ®Google Scholar
• O’Brien, P. J. , & Ellenberger, T. (2004). Dissecting the broad substrate specificity of human 3-methyladenine-DNA glycosylase. Journal of Biological Chemistry , 279 , 9750–9757.10.1074/jbc.M312232200
   PubMed Web of Science ®Google Scholar
• Connor, T. R. (1993). Purification and characterization of human 3-methyladenine-DNA glycosylase. Nucleic Acids Research , 21 , 5561–5569.10.1093/nar/21.24.5561
   PubMed Web of Science ®Google Scholar
• O’Connor, T. R. , Boiteux, S. , & Laval, J. (1988). Ring-opened 7-methylguanine residues in DNA are a block to in vitro DNA synthesis. Nucleic Acids Research , 16 , 5879–5894.10.1093/nar/16.13.5879
   PubMed Web of Science ®Google Scholar
• Patel, D. J. , & Hilbers, C. W. (1975). Proton nuclear magnetic resonance investigations of fraying in double-stranded d-ApTpGpCpApT in aqueous solution. Biochemistry , 14 , 2651–2656.10.1021/bi00683a014
   PubMed Web of Science ®Google Scholar
• Plateau, P. , & Gueron, M. (1982). Exchangeable proton NMR without base-line distorsion, using new strong-pulse sequences. Journal of the American Chemical Society , 104 , 7310–7311.10.1021/ja00389a067
   Web of Science ®Google Scholar
• Rachofsky, E. L. , Osman, R. , & Ross, J. B. A. (2001). Probing structure and dynamics of DNA with 2-aminopurine: Effects of local environment on fluorescence. Biochemistry , 40 , 946–956.10.1021/bi001664o
   PubMed Web of Science ®Google Scholar
• Roos, W. P. , & Kaina, B. (2006). DNA damage-induced cell death by apoptosis. Trends in Molecular Medicine , 12 , 440–450.10.1016/j.molmed.2006.07.007
   PubMed Web of Science ®Google Scholar
• Russu, I. M. (2004). Probing site-specific energetics in proteins and nucleic acids by hydrogen exchange and nuclear magnetic resonance spectroscopy. Methods in Enzymology , 379 , 152–175.10.1016/S0076-6879(04)79009-6
   PubMed Web of Science ®Google Scholar
• Saparbaev, M. , Kleibl, K. , & Laval, J. (1995). Escherichia coli, Saccharomyces cerevisiae, rat and human 3-methyladenine DNA glycosylases repair 1, N6-ethenoadenine when present in DNA. Nucleic Acids Research , 23 , 3750–3755.10.1093/nar/23.18.3750
   PubMed Web of Science ®Google Scholar
• Saparbaev, M. , Langouet, S. , Privezentzev, C. V. , Guengerich, F. P. , Cai, H. , Elder, R. H. , & Laval, J. (2002). 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. Journal of Biological Chemistry , 277 , 26987–26993.10.1074/jbc.M111100200
   PubMed Web of Science ®Google Scholar
• Saparbaev, M. , Mani, J. C. , & Laval, J. (2000). Interactions of the human, rat, Saccharomyces cerevisiae and Escherichia coli 3-methyladenine-DNA glycosylases with DNA containing dIMP residues. Nucleic Acids Research , 28 , 1332–1339.10.1093/nar/28.6.1332
   PubMed Web of Science ®Google Scholar
• Sedgwick, B. , Bates, P. A. , Paik, J. , Jacobs, S. C. , & Lindahl, T. (2007). Repair of alkylated DNA: recent advances. DNA Repair , 6 , 429–442.10.1016/j.dnarep.2006.10.005
   PubMed Web of Science ®Google Scholar
• Setser, J. W. , Lingaraju, G. M. , Davis, C. A. , Samson, L. D. , & Drennan, C. L. (2012). Searching for DNA lesions: Structural evidence for lower- and higher-affinity DNA binding conformations of human alkyladenine DNA glycosylase. Biochemistry , 51 , 382–390.10.1021/bi201484k
   PubMed Web of Science ®Google Scholar
• Stivers, J. T. , Pankiewicz, K. W. , & Watanabe, K. A. (1999). Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry , 38 , 952–963.10.1021/bi9818669
   PubMed Web of Science ®Google Scholar
• Sun, X. , & Lee, J. K. (2010). Stability of DNA duplexes containing hypoxanthine (inosine): Gas versus solution phase and biological implications. The Journal of Organic Chemistry , 75 , 1848–1854.10.1021/jo9023683
   PubMed Web of Science ®Google Scholar
• Taylor, J. S. , Garrett, D. S. , Brockie, I. R. , Svoboda, D. L. , & Telser, J. (1990). Proton NMR assignment and melting temperature study of cis-syn and trans-syn thymine dimer containing duplexes of d(CGTATTATGC).cntdot.d(GCATAATACG). Biochemistry , 29 , 8858–8866.10.1021/bi00489a049
   PubMed Web of Science ®Google Scholar
• Timofeyeva, N. A. , Koval, V. V. , Ishchenko, A. A. , Saparbaev, M. K. , & Fedorova, O. S. (2011). Lys98 substitution in human AP endonuclease 1 affects the kinetic mechanism of enzyme action in base excision and nucleotide incision repair pathways. PLoS ONE , 6 , e24063.10.1371/journal.pone.0024063
   PubMed Web of Science ®Google Scholar
• Vallur, A. C. , Maher, R. L. , & Bloom, L. B. (2005). The efficiency of hypoxanthine excision by alkyladenine DNA glycosylase is altered by changes in nearest neighbor bases. DNA Repair , 4 , 1088–1098.10.1016/j.dnarep.2005.05.008
   PubMed Web of Science ®Google Scholar
• Wallace, S. S. (2002). Biological consequences of free radical-damaged DNA bases. Free Radical Biology and Medicine , 33 , 1–14.10.1016/S0891-5849(02)00827-4
   PubMed Web of Science ®Google Scholar
• Wenke, B. B. , Huiting, L. N. , Frankel, E. B. , Lane, B. F. , & Núñez, M. E. (2013). Base pair opening in a deoxynucleotide duplex containing a cis-syn thymine cyclobutane dimer lesion. Biochemistry , 52 , 9275–9285.10.1021/bi401312r
   PubMed Web of Science ®Google Scholar
• Wolfe, A. E. , & O’Brien, P. J. (2009). Kinetic mechanism for the flipping and excision of 1, N(6)-ethenoadenine by human alkyladenine DNA glycosylase. Biochemistry , 48 , 11357–11369.10.1021/bi9015082
   PubMed Web of Science ®Google Scholar