A thymine isostere in the templating position disrupts assembly of the closed DNA polymerase β ternary complex

Biochemistry

Volumn 44, Issue 46, 2005, Pages 15230-15237

  Kirby, Thomas W ^a   DeRose, Eugene F ^a   Beard, William A ^a   Wilson, Samuel H ^a   London, Robert E ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; CATALYSIS; CONFORMATIONS; DNA; GENES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYMERIZATION;

DNA POLYMERIZATION; NUCLEOTIDES; POLYMERASE FIDELITY; THYMINE ISOSTERE;

ENZYMES;

DIFLUOROTOLUENE; DNA DIRECTED DNA POLYMERASE BETA; LYASE; METHIONINE; NUCLEOTIDE; THYMINE; TOLUENE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; CATALYSIS; COMPLEX FORMATION; CONFORMATION; CONFORMATIONAL TRANSITION; DNA REPAIR; GENOMIC INSTABILITY; HUMAN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; STEREOCHEMISTRY;

ANIMALS; BASE SEQUENCE; DNA POLYMERASE BETA; METHIONINE; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RATS; TEMPLATES, GENETIC; THYMINE; TOLUENE;

EID: 27944436617     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0511742     Document Type: Article

References (35)

1. Beard, W. A., and Wilson, S. H. (2000) Structural design of a eukaryotic DNA repair polymerase: DNA polymerase β, Mutat. Res. 460, 231-244.
2. Sawaya, M. R., Prasad, R., Wilson, S. H., Kraut, J., Pelletier, H. (1997) Crystal structures of human DNA polymerase β complexed with gapped and nicked DNA: Evidence for an induced fit mechanism, Biochemistry 36, 11205-11215.
3. Vande Berg, B. J., Beard, W. A., and Wilson, S. H. (2001) DNA structure and aspartate 276 influence nucleotide binding to human DNA polymerase β: Implication for the identity of the rate-limiting conformational change, J. Biol. Chem. 276, 3408-3416.
4. Yang, L., Beard, W. A., Wilson, S. H., Broyde, S., and Schlick, T. (2002) Polymerase β simulations suggest that Arg258 rotation is a slow step rather than large subdomain motions per se, J. Mol. Biol. 317, 679-699.
5. Yang, L., Beard, W. A., Wilson, S. H., Broyde, S., and Schlick, T. (2004) Highly organized but pliant active site of DNA polymerase β: Compensatory mechanisms in mutant enzymes revealed by dynamics simulations and energy analyses, Biophys. J. 86, 3392-3408.
6. Kim, S.-J., Beard, W. A., Harvey, J., Shock, D. D., Knutson, J. R., and Wilson, S. H. (2003) Rapid segmental and subdomain motions of DNA polymerase β, J. Biol Chem. 278, 5072-5081.
7. Beard, W. A., Shock, D. D., and Wilson, S. H. (2004) Influence of DNA structure on DNA polymerase β active site function: Extension of mutagenic DNA intermediates, J. Biol. Chem. 279, 31921-31929.
8. 13C] methionine-labeled DNA polymerase β, Biochemistry 43, 8911-8922.
9. Prasad, R., Beard, W. A., and Wilson, S. H. (1994) Studies of gapped DNA substrate binding by mammalian DNA polymerase β: Dependence on 5′-phosphate group, J. Biol, Chem. 269, 18096-18101.
10. Kool, E. T. (2002) Active site tightness and substrate fit in DNA replication, Annu. Rev. Biochem. 71, 191-219.
11. Morales, J. C., and Kool, E. T. (2000) Varied molecular interactions at the active sites of several DNA polymerases: Non-polar isosteres as probes, J. Am. Chem. Soc. 122, 1001-1007.
12. Schweitzer, B. A., and Kool, E. T. (1994) Aromatic nonpolar nucleosides as hydrophobic isosteres of pyrimidine and purine nucleosides, J. Org. Chem. 59, 7238-7242.
13. John, B. K., Plant, D., and Hurd, R. E. (1993) Improved proton-detected heteronuclear correlation using gradient-enhanced Z and ZZ filters, J. Magn. Reson. 101, 113-117.
14. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: A multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
15. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
16. Zhu, G., and Bax, A. (1992) Improved linear prediction of damped NMR signals using modified forward backward linear prediction, J. Magn. Reson. 100, 202-207.
17. 15N chemical shifts, J. Biomol. NMR 26, 215-240.
18. Xu, X. P., and Case, D. A. (2001) Automated prediction of N-15, C-13(α), C-13(β) and C-13′ chemical shifts in proteins using a density functional database, J. Biomol. NMR 21, 321-333.
19. Xu, X. P., and Case, D. A. (2002) Probing multiple effects on N-15, C-13α, C-13β, and C-13′ chemical shifts in peptides using density functional theory, Biopolymers 65, 408-423.
20. Hirao, I., Nishimura, Y., Naraoka, T., Watanabe, K., Arata, Y., and Miura, K. (1989) Extraordinary stable structure of short single-stranded-DNA fragments containing a specific base sequence-d(GCGAAGC), Nucleic Acids Res. 17, 2223-2231.
21. Williams, H. E. L., Colgrave, M. L., and Searle, M. S. (2002) Drug recognition of a single DNA strand break; nogalamycin intercalation between coaxially stacked hairpins, Eur. J. Biochem. 269, 1726-1733.
22. Beard, W. A., and Wilson, S. H. (2003) Structural insights into the origins of DNA polymerase fidelity, Structure 11, 489-496.
23. Krahn, J. M., Beard, W. A., Miller, H., Grollman, A. P., and Wilson, S. H. (2003) Structure of DNA polymerase β with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential, Structure 11, 121-127.
24. Krahn, J. M., Beard, W. A., and Wilson, S. H. (2004) Structural insights into DNA polymerase deterrents for misincorporation support an induced-fit mechanism for fidelity, Structure 12, 1823-1832.
25. Beard, W. A., and Wilson, S. H. (2001) DNA lesion bypass polymerases open up, Structure 9, 759-764.
26. Garcia-Diaz, M., Bebenek, K., Krahn, J. M., Blanco, L., Kunkel, T. A., and Pedersen, L. C. (2004) A structural solution for the DNA polymerase λ-dependent repair of DNA gaps with minimal homology, Mol. Cell 13, 561-572.
27. Moran, S., Ren, R. X.-F., and Kool, E. T. (1997) A thymidine triphosphate shape analog lacking Watson-Crick pairing ability is replicated with high sequence selectivity, Proc. Natl. Acad. Sci. U.S.A. 94, 10506-10511.
28. Moran, S., Ren, R. X.-F., Rumney, S., IV, and Kool, E. T. (1997) Difluorotoluene, a nonpolar isostere for thymine, codes specifically and efficiently for adenine in DNA replication, J. Am. Chem. Soc. 119, 2056-2057.
29. Yang, L., Arora, K., Beard, W. A., Wilson, S. H., and Schlick, T. (2004) Critical role of magnesium ions in DNA polymerase β's closing and active site assembly, J. Am. Chem. Soc. 126, 8441-8453.
30. 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. (1996) Enzyme-DNA interactions required for efficient nucleotide incorporation and discrimination in human DNA polymerase β, J. Biol. Chem. 271, 12141-12144.
31. Beard, W. A., Shock, D. D., Vande Berg, B. J., and Wilson, S. H. (2002) Efficiency of correct nucleotide insertion governs DNA polymerase fidelity, J. Biol. Chem. 277, 47393-47398.
32. Osheroff, W. P., Beard, W. A., Wilson, S. H., and Kunkel, T. A. (1999) Base substitution specificity of DNA polymerase β depends on interactions in the DNA minor groove, J. Biol. Chem. 274, 20749-20752.
33. Osheroff, W. P., Beard, W. A., Yin, S., Wilson, S. H., and Kunkel, T. A. (2000) Minor groove interactions at the DNA polymerase β active site modulate single-base deletion error rates, J. Biol. Chem. 275, 28033-28038.
34. Dzantiev, L., Alekseyev, Y. O., Morales, J. C., Kool, E. T., and Romano, L. J. (2001) Significance of nucleobase shape complementarity and hydrogen bonding in the formation and stability of the closed polymerase-DNA complex, Biochemistry 40, 3215-3221.
35. Beard, W. A., Shock, D. D., Yang, X.-P., DeLauder, S. F., and Wilson, S. H. (2002) Loss of DNA polymerase β stacking interactions with templating purines, but not pyrimidines, alters catalytic efficiency and fidelity, J. Biol. Chem. 277, 8235-8242.