Glycosidic Bond Cleavage in DNA Nucleosides: Effect of Nucleobase Damage and Activation on the Mechanism and Barrier

Journal of Physical Chemistry B

Volumn 119, Issue 51, 2015, Pages 15601-15612

  Lenz, Stefan A P ^a   Kellie, Jennifer L ^a   Wetmore, Stacey D ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; CHEMICAL ACTIVATION; CHEMICAL BONDS; DENSITY FUNCTIONAL THEORY; DISSOCIATION; REDUCTION; REPAIR; STABILITY; SUGARS; SURFACE REACTIONS;

ALKYLATION PRODUCTS; BASE EXCISION REPAIRS; COMPUTATIONALLY EFFICIENT; DELETERIOUS EFFECTS; DISSOCIATIVE PATHWAYS; DNA-REPAIR ENZYMES; GLYCOSIDIC BOND CLEAVAGE; INTRINSIC STABILITY;

DNA;

DNA; GLYCOSIDE;

ALKYLATION; DEAMINATION; DNA DAMAGE; METABOLISM; OXIDATION REDUCTION REACTION;

ALKYLATION; DEAMINATION; DNA; DNA DAMAGE; GLYCOSIDES; OXIDATION-REDUCTION;

EID: 84952342375     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b10337     Document Type: Article

References (84)

1. Wallace, S. S.; Murphy, D. L.; Sweasy, J. B. Base Excision Repair and Cancer Cancer Lett. 2012, 327 (1-2) 73-89 10.1016/j.canlet.2011.12.038
2. Svilar, D.; Goellner, E. M.; Almeida, K. H.; Sobol, R. W. Base Excision Repair and Lesion-Dependent Subpathways for Repair of Oxidative DNA Damage Antioxid. Redox Signaling 2011, 14 (12) 2491-2507 10.1089/ars.2010.3466
3. Dizdaroglu, M. Oxidatively Induced DNA Damage: Mechanisms, Repair and Disease Cancer Lett. 2012, 327 (1-2) 26-47 10.1016/j.canlet.2012.01.016
4. Jacobs, A. L.; Schar, P. DNA Glycosylases: In DNA Repair and Beyond Chromosoma 2012, 121 (1) 1-20 10.1007/s00412-011-0347-4
5. Berti, P. J.; McCann, J. A. B. Toward a Detailed Understanding of Base Excision Repair Enzymes: Transition State and Mechanistic Analyses of N-Glycoside Hydrolysis and N-Glycoside Transfer Chem. Rev. 2006, 106 (2) 506-555 10.1021/cr040461t
6. McCann, J. A. B.; Berti, P. J. Transition-State Analysis of the DNA Repair Enzyme MutY J. Am. Chem. Soc. 2008, 130 (17) 5789-5797 10.1021/ja711363s
7. O'Brien, P. J.; Ellenberger, T. Dissecting the Broad Substrate Specificity of Human 3-Methyladenine-DNA Glycosylase J. Biol. Chem. 2004, 279 (11) 9750-9757 10.1074/jbc.M312232200
8. Chu, A. M.; Fettinger, J. C.; David, S. S. Profiling Base Excision Repair Glycosylases with Synthesized Transition State Analogs Bioorg. Med. Chem. Lett. 2011, 21 (17) 4969-4972 10.1016/j.bmcl.2011.05.085
9. Zharkov, D. O.; Mechetin, G. V.; Nevinsky, G. A. Uracil-DNA Glycosylase: Structural, Thermodynamic and Kinetic Aspects of Lesion Search and Recognition Mutat. Res., Fundam. Mol. Mech. Mutagen. 2010, 685 (1-2) 11-20 10.1016/j.mrfmmm.2009.10.017
10. Drohat, A. C.; Jagadeesh, J.; Ferguson, E.; Stivers, J. T. Role of Electrophilic and General Base Catalysis in the Mechanism of Escherichia Coli Uracil DNA Glycosylase Biochemistry 1999, 38 (37) 11866-11875 10.1021/bi9910878
11. Lindahl, T. An N-Glycosidase from Eschirichia Coli That Releases Free Uracil from DNA Containing Deaminated Cytosine Residues Proc. Natl. Acad. Sci. U. S. A. 1974, 71 (9) 3649-3653 10.1073/pnas.71.9.3649
12. Lee, S.; Verdine, G. L. Atomic Substitution Reveals the Structural Basis for Substrate Adenine Recognition and Removal by Adenine DNA Glycosylase Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (44) 18497-18502 10.1073/pnas.0902908106
13. Dong, L.; Mi, R.; Glass, R. A.; Barry, J. N.; Cao, W. Repair of Deaminated Base Damage by Schizosaccharomyces Pombe Thymine DNA Glycosylase DNA Repair 2008, 7 (12) 1962-1972 10.1016/j.dnarep.2008.08.006
14. Hang, B.; Guliaev, A. B. Substrate Specificity of Human Thymine-DNA Glycosylase on Exocyclic Cytosine Adducts Chem.-Biol. Interact. 2007, 165 (3) 230-238 10.1016/j.cbi.2006.12.013
15. Parikh, S. S.; Walcher, G.; Jones, G. D.; Slupphaug, G.; Krokan, H. E.; Blackburn, G. M.; Tainer, J. A. Uracil-DNA Glycosylase-DNA Substrate and Product Structures: Conformational Strain Promotes Catalytic Efficiency by Coupled Stereoelectronic Effects Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (10) 5083-5088 10.1073/pnas.97.10.5083
16. Faucher, F.; Doublié, S.; Jia, Z. 8-Oxoguanine DNA Glycosylases: One Lesion, Three Subfamilies Int. J. Mol. Sci. 2012, 13 (6) 6711-6729 10.3390/ijms13066711
17. Koval, V. V.; Knorre, D. G.; Fedorova, O. S. Structural Features of the Interaction between Human 8-Oxoguanine DNA Glycosylase hOgg1 and DNA Acta Naturae 2014, 6 (3) 52-65
18. Lau, A. Y.; Wyatt, M. D.; Glassner, B. J.; Samson, L. D.; Ellenberger, T. Molecular Basis for Discriminating between Normal and Damaged Bases by the Human Alkyladenine Glycosylase, Aag Proc. Natl. Acad. Sci. U. S. A. 2000, 97 (25) 13573-13578 10.1073/pnas.97.25.13573
19. 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. 2012, 287 (6) 4288-4298 10.1074/jbc.M111.315309
20. Zharkov, D. O.; Rosenquist, T. A.; Gerchman, S. E.; Grollman, A. P. Substrate Specificity and Reaction Mechanism of Murine 8-Oxoguanine-DNA Glycosylase J. Biol. Chem. 2000, 275 (37) 28607-28617 10.1074/jbc.M002441200
21. Brunk, E.; Arey, J. S.; Rothlisberger, U. Role of Environment for Catalysis of the DNA Repair Enzyme MutY J. Am. Chem. Soc. 2012, 134 (20) 8608-8616 10.1021/ja301714j
22. Rutledge, L. R.; Wetmore, S. D. Modeling the Chemical Step Utilized by Human Alkyladenine DNA Glycosylase: A Concerted Mechanism Aids in Selectively Excising Damaged Purines J. Am. Chem. Soc. 2011, 133, 16258-16269 10.1021/ja207181c
23. Kellie, J. L.; Wilson, K. A.; Wetmore, S. D. Standard Role for a Conserved Aspartate or More Direct Involvement in Deglycosylation? An ONIOM and MD Investigation of Adenine-DNA Glycosylase Biochemistry 2013, 52 (48) 8753-8765 10.1021/bi401310w
24. Alexandrova, A. N. Promiscuous DNA Alkyladenine Glycosylase Dramatically Favors a Bound Lesion over Undamaged Adenine Biophys. Chem. 2010, 152 (1-3) 118-127 10.1016/j.bpc.2010.08.007
25. Kellie, J. L.; Wilson, K. A.; Wetmore, S. D. An ONIOM and MD Investigation of Possible Monofunctional Activity of Human 8-Oxoguanine-DNA Glycosylase (hOgg1) J. Phys. Chem. B 2015, 119 (25) 8013-8023 10.1021/acs.jpcb.5b04051
26. Sadeghian, K.; Ochsenfeld, C. Unraveling the Base Excision Repair Mechanism of Human DNA Glycosylase J. Am. Chem. Soc. 2015, 137 (31) 9824-9831 10.1021/jacs.5b01449
27. Blank, I. D.; Sadeghian, K.; Ochsenfeld, C. A Base-Independent Repair Mechanism for DNA Glycosylase¯No Discrimination within the Active Site Sci. Rep. 2015, 5, 10369 10.1038/srep10369
28. Sadeghian, K.; Flaig, D.; Blank, I. D.; Schneider, S.; Strasser, R.; Stathis, D.; Winnacker, M.; Carell, T.; Ochsenfeld, C. Ribose-Protonated DNA Base Excision Repair: A Combined Theoretical and Experimental Study Angew. Chem., Int. Ed. 2014, 53 (38) 10044-10048 10.1002/anie.201403334
29. Kanaan, N.; Crehuet, R.; Imhof, P. Mechanism of the Glycosidic Bond Cleavage of Mismatched Thymine in Human Thymine DNA Glycosylase Revealed by Classical Molecular Dynamics and Quantum Mechanical/Molecular Mechanical Calculations J. Phys. Chem. B 2015, 119 (38) 12365-12380 10.1021/acs.jpcb.5b05496
30. Przybylski, J. L.; Wetmore, S. D. A QM/QM Investigation of the hUNG2 Reaction Surface: The Untold Tale of a Catalytic Residue Biochemistry 2011, 50 (19) 4218-4227 10.1021/bi2003394
31. Millen, A. L.; Archibald, L. A. B.; Hunter, K. C.; Wetmore, S. D. A Kinetic and Thermodynamic Study of the Glycosidic Bond Cleavage in Deoxyuridine J. Phys. Chem. B 2007, 111 (14) 3800-3812 10.1021/jp063841m
32. Millen, A. L.; Wetmore, S. D. Glycosidic Bond Cleavage in Deoxynucleotides-a Density Functional Study Can. J. Chem. 2009, 87 (7) 850-863 10.1139/V09-024
33. Przybylski, J. L.; Wetmore, S. D. Designing an Appropriate Computational Model for DNA Nucleoside Hydrolysis: A Case Study of 2′-Deoxyuridine J. Phys. Chem. B 2009, 113 (18) 6533-6542 10.1021/jp810472q
34. Przybylski, J. L.; Wetmore, S. D. Modeling the Dissociative Hydrolysis of the Natural DNA Nucleosides J. Phys. Chem. B 2010, 114 (2) 1104-1113 10.1021/jp9098717
35. Shim, E. J.; Przybylski, J. L.; Wetmore, S. D. Effects of Nucleophile, Oxidative Damage, and Nucleobase Orientation on the Glycosidic Bond Cleavage in Deoxyguanosine J. Phys. Chem. B 2010, 114 (6) 2319-2326 10.1021/jp9113656
36. Kellie, J. L.; Navarro-Whyte, L.; Carvey, M. T.; Wetmore, S. D. Combined Effects of π-π Stacking and Hydrogen Bonding on the (N1) Acidity of Uracil and Hydrolysis of 2′-Deoxyuridine J. Phys. Chem. B 2012, 116 (8) 2622-2632 10.1021/jp2121627
37. Lenz, S. A. P.; Kellie, J. L.; Wetmore, S. D. Glycosidic Bond Cleavage in Deoxynucleotides: Effects of Solvent and the DNA Phosphate Backbone in the Computational Model J. Phys. Chem. B 2012, 116 (49) 14275-14284 10.1021/jp3096677
38. Navarro-Whyte, L.; Kellie, J. L.; Lenz, S. A. P.; Wetmore, S. D. Hydrolysis of the Damaged Deoxythymidine Glycol Nucleoside and Comparison to Canonical DNA Phys. Chem. Chem. Phys. 2013, 15 (44) 19343-19352 10.1039/c3cp53217h
39. Sowlati-Hashjin, S.; Wetmore, S. D. Computational Investigation of Glycosylase and β-Lyase Activity Facilitated by Proline: Applications to Fpg and Comparisons to hOgg1 J. Phys. Chem. B 2014, 118 (50) 14566-14577 10.1021/jp507783d
40. Kellie, J. L.; Wetmore, S. D. Mechanistic and Conformational Flexibility of the Covalent Linkage Formed During β-Lyase Activity on an AP-Site: Application to hOgg1 J. Phys. Chem. B 2012, 116, 10786 10.1021/jp306344g
41. Zheng, Y.; Xue, Y.; Yan, S. G. The Effects of Oxidation and Protonation on the N-Glycosidic Bond Stability of 8-Oxo-2′-Deoxyguanosine: DFT Study J. Mol. Struct.: THEOCHEM 2008, 860 (1-3) 52-57 10.1016/j.theochem.2008.03.014
42. Zheng, Y.; Xue, Y.; Yan, G. S. The Influences of Oxidation and Cationization on the N-Glycosidic Bond Stability of 8-Oxo-2′-Deoxyadenosine-a Theoretical Study J. Theor. Comput. Chem. 2009, 8 (6) 1253-1264 10.1142/S0219633609005349
43. Chen, Z. Q.; Xue, Y. Theoretical Investigations on the Thermal Decomposition Mechanism of 5-Hydroxy-6-Hydroperoxy-5,6-Dihydrothymidine in Water J. Phys. Chem. B 2010, 114 (39) 12641-12654 10.1021/jp100933d
44. Chen, Z. Q.; Zhang, C. H.; Xue, Y. Theoretical Studies on the Thermodynamics and Kinetics of the N-Glycosidic Bond Cleavage in Deoxythymidine Glycol J. Phys. Chem. B 2009, 113 (30) 10409-10420 10.1021/jp903334j
45. O'Brien, P. J.; Ellenberger, T. Human Alkyladenine DNA Glycosylase Uses Acid-Base Catalysis for Selective Excision of Damaged Purines Biochemistry 2003, 42 (42) 12418-12429 10.1021/bi035177v
46. Lindahl, T.; Ljungquist, S.; Siegert, W.; Nyberg, B.; Sperens, B. DNA N-Glycosidases-Properties of Uracil-DNA Glycosidase from Escherichia-Coli J. Biol. Chem. 1977, 252 (10) 3286-3294
47. Krokan, H.; Wittwer, C. U. Uracil DNA-Glycosylase from Hela-Cells-General-Properties, Substrate-Specificity and Effect of Uracil Analogs Nucleic Acids Res. 1981, 9 (11) 2599-2614 10.1093/nar/9.11.2599
48. Kavli, B.; Sundheim, O.; Akbari, M.; Otterlei, M.; Nilsen, H.; Skorpen, F.; Aas, P. A.; Hagen, L.; Krokan, H. E.; Slupphaug, G. hUNG2 Is the Major Repair Enzyme for Removal of Uracil from U:A Matches, U:G Mismatches, and U in Single-Stranded DNA, with Hsmug1 as a Broad Specificity Backup J. Biol. Chem. 2002, 277 (42) 39926-39936 10.1074/jbc.M207107200
49. Waters, T. R.; Swann, P. F. Thymine-DNA Glycosylase and G to a Transition Mutations at CpG Sites Mutat. Res., Rev. Mutat. Res. 2000, 462 (2-3) 137-147 10.1016/S1383-5742(00)00031-4
50. Liu, P. F.; Burdzy, A.; Sowers, L. C. Substrate Recognition by a Family of Uracil-DNA Glycosylases: UNG, MUG, and TDG Chem. Res. Toxicol. 2002, 15 (8) 1001-1009 10.1021/tx020030a
51. Wu, P. Y.; Qiu, C.; Sohail, A.; Zhang, X.; Bhagwat, A. S.; Cheng, X. D. Mismatch Repair in Methylated DNA-Structure and Activity of the Mismatch-Specific Thymine Glycosylase Domain of Methyl-CpG-Binding Protein Mbd4 J. Biol. Chem. 2003, 278 (7) 5285-5291 10.1074/jbc.M210884200
52. Francis, A. W.; Helquist, S. A.; Kool, E. T.; David, S. S. Probing the Requirements for Recognition and Catalysis in Fpg and MutY with Nonpolar Adenine Isosteres J. Am. Chem. Soc. 2003, 125 (52) 16235-16242 10.1021/ja0374426
53. Livingston, A. L.; O'Shea, V. L.; Kim, T.; Kool, E. T.; David, S. S. Unnatural Substrates Reveal the Importance of 8-Oxoguanine for in Vivo Mismatch Repair by MutY Nat. Chem. Biol. 2008, 4 (1) 51-58 10.1038/nchembio.2007.40
54. Hamm, M. L.; Gill, T. J.; Nicolson, S. C.; Summers, M. R. Substrate Specificity of Fpg (MutM) and hOgg1, Two Repair Glycosylases J. Am. Chem. Soc. 2007, 129 (25) 7724-7725 10.1021/ja0716453
55. Nevinsky, G. A. Structural, Thermodynamic, and Kinetic Basis for the Activities of Some Nucleic Acid Repair Enzymes J. Mol. Recognit. 2011, 24 (4) 656-677 10.1002/jmr.1096
56. Lau, A. Y.; Scharer, O. D.; Samson, L.; Verdine, G. L.; Ellenberger, E. Crystal Structure of a Human Alkylbase-DNA Repair Enzyme Complexed to DNA: Mechanisms for Nucleotide Flipping and Base Excision Cell 1998, 95 (2) 249-258 10.1016/S0092-8674(00)81755-9
57. Fromme, J. C.; Banerjee, A.; Huang, S. J.; Verdine, G. L. Structural Basis for Removal of Adenine Mispaired with 8-Oxoguanine by MutY Adenine DNA Glycosylase Nat. Mater. 2004, 427 (6975) 652-656 10.1038/nature02306
58. Parker, J. B.; Stivers, J. T. Uracil DNA Glycosylase: Revisiting Substrate-Assisted Catalysis by DNA Phosphate Anions Biochemistry 2008, 47 (33) 8614-8622 10.1021/bi800854g
59. Chen, X.-Y.; Berti, P. J.; Schramm, V. L. Transition-State Analysis for Depurination of DNA by Ricin A-Chain J. Am. Chem. Soc. 2000, 122 (28) 6527-6534 10.1021/ja992751a
60. Rios-Font, R.; Bertran, J.; Sodupe, M.; Rodriguez-Santiago, L. On the Mechanism of the N-Glycosydic Bond Hydrolysis of 2′-Deoxyguanosine: Insights from First Principles Calculations Theor. Chem. Acc. 2011, 128 (4-6) 619-626 10.1007/s00214-010-0826-3
61. Shapiro, R.; Kang, S. Uncatalyzed Hydrolysis of Deoxyuridine, Thymidine, and 5-Bromodeoxyuridine Biochemistry 1969, 8 (5) 1806-1810 10.1021/bi00833a004
62. Garrett, E. R.; Seydel, J. K.; Sharpen, A. J. Acid-Catalyzed Solvolysis of Pyrimidine Nucleosides J. Org. Chem. 1966, 31 (7) 2219-2227 10.1021/jo01345a033
63. Lindahl, T.; Karlstrom, O. Heat-Induced Depyrimidination of Deoxyribonucleic Acid in Neutral Solution Biochemistry 1973, 12 (25) 5151-5154 10.1021/bi00749a020
64. Schroeder, G. K.; Wolfenden, R. Rates of Spontaneous Disintegration of DNA and the Rate Enhancements Produced by DNA Glycosylases and Deaminases Biochemistry 2007, 46 (47) 13638-13647 10.1021/bi701480f
65. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; et al., Gaussian 09, Revision A.02; Gaussian, Inc.: Wallingford, CT, 2009.
66. 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 2009, 113 (18) 6378-6396 10.1021/jp810292n
67. Shapiro, R.; Danzig, M. Acidic Hydrolysis of Deoxycytidine and Deoxyuridine Derivatives. General Mechanism of Deoxyribonucleoside Hydrolysis Biochemistry 1972, 11 (1) 23-29 10.1021/bi00751a005
68. Cramer, C. J. Essentials of Computational Chemistry: Theories and Models; Wiley: Chichester, U.K., 2004.
69. Suzuki, T.; Yoshida, M.; Yamada, M.; Ide, H.; Kobayashi, M.; Kanaori, K.; Tajima, K.; Makino, K. Misincorporation of 2′-Deoxyoxanosine 5′-Triphosphate by DNA Polymerases and Its Implication for Mutagenesis Biochemistry 1998, 37 (33) 11592-11598 10.1021/bi980971f
70. Vongchampa, V.; Dong, M.; Gingipalli, L.; Dedon, P. Stability of 2 ′-Deoxyxanthosine in DNA Nucleic Acids Res. 2003, 31 (3) 1045-1051 10.1093/nar/gkg177
71. Norman, D. P. G.; Chung, S. J.; Verdine, G. L. Structural and Biochemical Exploration of a Critical Amino Acid in Human 8-Oxoguanine Glycosylase Biochemistry 2003, 42 (6) 1564-1572 10.1021/bi026823d
72. Norman, D. P. G.; Bruner, S. D.; Verdine, G. L. Coupling of Substrate Recognition and Catalysis by a Human Base-Excision DNA Repair Protein J. Am. Chem. Soc. 2001, 123 (2) 359-360 10.1021/ja003144m
73. Bruner, S. D.; Norman, D. P. G.; Verdine, G. L. Structural Basis for Recognition and Repair of the Endogenous Mutagen 8-Oxoguanine in DNA Nature 2000, 403 (6772) 859-866 10.1038/35002510
74. Yoon, J.-H.; Iwai, S.; O'Connor, T. R.; Pfeifer, G. P. Human Thymine DNA Glycosylase (TDG) and Methyl-Cpg-Binding Protein 4 (MBD4) Excise Thymine Glycol (Tg) from a Tg:G Mispair Nucleic Acids Res. 2003, 31 (18) 5399-5404 10.1093/nar/gkg730
75. Ocampo-Hafalla, M. T.; Altamirano, A.; Basu, A. K.; Chan, M. K.; Ocampo, J. E. A.; Cummings, A.; Boorstein, R. J.; Cunningham, R. P.; Teebor, G. W. Repair of Thymine Glycol by hNTH1 and hNEIL1 Is Modulated by Base Pairing and Cis-Trans Epimerization DNA Repair 2006, 5 (4) 444-454 10.1016/j.dnarep.2005.12.004
76. Hardeland, U.; Bentele, M.; Jiricny, J.; Schär, P. Separating Substrate Recognition from Base Hydrolysis in Human Thymine DNA Glycosylase by Mutational Analysis J. Biol. Chem. 2000, 275 (43) 33449-33456 10.1074/jbc.M005095200
77. Parker, J. B.; Stivers, J. T. Dynamics of Uracil and 5-Fluorouracil in DNA Biochemistry 2011, 50 (5) 612-617 10.1021/bi101536k
78. Rosler, A.; Panayotou, G.; Hornby, D. P.; Barlow, T.; Brown, T.; Pearl, L. H.; Savva, R.; Blackburn, G. M. The Mechanism of DNA Repair by Uracil-DNA Glycosylase: Studies Using Nucleotide Analogues Nucleosides, Nucleotides Nucleic Acids 2000, 19 (10-12) 1505-1516 10.1080/15257770008045442
79. Lu, A. L.; Yuen, D. S.; Cillo, J. Catalytic Mechanism and DNA Substrate Recognition of Escherichia Coli Muty Protein J. Biol. Chem. 1996, 271 (39) 24138-24143 10.1074/jbc.271.39.24138
80. Lu, A. L.; Li, X.; Gu, Y.; Wright, P. M.; Chang, D.-Y. Repair of Oxidative DNA Damage: Mechanisms and Functions Cell Biochem. Biophys. 2001, 35 (2) 141-170 10.1385/CBB:35:2:141
81. Roldan-Arjona, T.; Wei, Y. F.; Carter, K. C.; Klungland, A.; Anselmino, C.; Wang, R. P.; Augustus, M.; Lindahl, T. Molecular Cloning and Functional Expression of a Human Cdna Encoding the Antimutator Enzyme 8-Hydroxyguanine-DNA Glycosylase Proc. Natl. Acad. Sci. U. S. A. 1997, 94 (15) 8016-8020 10.1073/pnas.94.15.8016
82. Fromme, J. C.; Verdine, G. L. DNA Lesion Recognition by the Bacterial Repair Enzyme MutM J. Biol. Chem. 2003, 278 (51) 51543-51548 10.1074/jbc.M307768200
83. Slupphaug, G.; Eftedal, I.; Kavli, B.; Bharati, S.; Helle, N. M.; Haug, T.; Levine, D. W.; Krokan, H. E. Properties of a Recombinant Human Uracil-DNA Glycosylase from the UNG Gene and Evidence That UNG Encodes the Major Uracil-DNA Glycosylase Biochemistry 1995, 34 (1) 128-138 10.1021/bi00001a016
84. Drohat, A. C.; Stivers, J. T. Escherichia Coli Uracil DNA Glycosylase: NMR Characterization of the Short Hydrogen Bond from His187 to Uracil O2 Biochemistry 2000, 39 (39) 11865-11875 10.1021/bi000922e