DNA polymerase β fidelity: Halomethylene-modified leaving groups in pre-steady-state kinetic analysis reveal differences at the chemical transition state

Biochemistry

Volumn 47, Issue 3, 2008, Pages 870-879

  Sucato, Christopher A ^a   Upton, Thomas G ^a   Kashemirov, Boris A ^a   Osuna, Jorge ^a   Oertell, Keriann ^a   Beard, William A ^c   Wilson, Samuel H ^c   Florián, Jan ^b   Warshel, Arieh ^a   McKenna, Charles E ^a   Goodman, Myron F ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CATALYSIS; CHEMICAL SHIFT; CORRELATION METHODS; DNA;

NUCLEOPHILIC ATTACK; NUCLEOTIDYL TRANSFER; PYROPHOSPHATE LEAVING-GROUP ELIMINATION;

ENZYME KINETICS;

CARBENE; DEUTERIUM; DNA DIRECTED DNA POLYMERASE BETA; FLUORINE; GUANOSINE TRIPHOSPHATE DERIVATIVE; HALOGEN; NUCLEOTIDE; PYROPHOSPHATE;

ARTICLE; BASE PAIRING; CONFORMATIONAL TRANSITION; DNA REPLICATION; ENERGY; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME MECHANISM; PKA; PRIORITY JOURNAL; STEADY STATE; STEREOSPECIFICITY;

BASE PAIR MISMATCH; CATALYSIS; CATALYTIC DOMAIN; DEOXYGUANINE NUCLEOTIDES; DEUTERIUM OXIDE; DIPHOSPHONATES; DNA; DNA POLYMERASE BETA; GUANOSINE TRIPHOSPHATE; HALOGENS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 38549165707     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7014162     Document Type: Article

References (51)

1. Batra, V. K., Beard, W. A., Shock, D. D., Pedersen, L. C., and Wilson, S. H. (2005) Nucleotide-induced DNA polymerase active site motions accommodating a mutagenic DNA intermediate, Structure 13, 1225-1233.
2. Batra, V. K., Shock, D. D., Prasad, R., Beard, W. A., Hou, E. W., Pedersen, L. C., Sayer, J. M., Yagi, H., Kumar, S., Jerina, D. M., and Wilson, S. H. (2006) Structure of DNA polymerase beta with a benzo[c]phenanthrene diol epoxide-adducted template exhibits inutagenic features, Proc. Natl. Acad. Sci. U.S.A. 103, 17231-17236.
3. Batra, V. K., Beard, W. A., Shock, D. D., Krahn, J. M., Pedersen, L. C., and Wilson, S. H. (2006) Magnesium-induced assembly of a complete DNA polymerase catalytic complex, Structure 14, 757-766.
4. McKenna, C. E., Kashemirov, B. A., Upton, T. G., Batra, V. K., Goodman, M. F., Pedersen, L. C., Beard, W. A., and Wilson, S. H. (2007) (R)-β,γ-fluoromethylene-dGTP-DNA ternary complex with DNA polymerase beta, J. Am. Chem. Soc. (in press).
5. Sucato, C. A., Upton, T. G., Kashemirov, B. A., Batra, V. K., Martinek, V., Xiang, Y., Beard, W. A., Pedersen, L. C., Wilson, S. H., McKenna, C. E., Florián, J., Warshel, A., and Goodman, M. F. (2007) Modifying the beta,gamma leaving-group bridging oxygen alters nucleotide incorporation efficiency, fidelity, and the catalytic mechanism of DNA polymerase β, Biochemistry 46, 461-471.
6. Bakhtina, M., Lee, S., Wang, Y., Dunlap, C., Lamarche, B., and Tsai, M. D. (2005) Use of viscogens, dNTPaS, and rhodium(III) as probes in stopped-flow experiments to obtain new evidence for the mechanism of catalysis by DNA polymerase β, Biochemistry 44, 5177-5187.
7. Bakhtina, M., Roettger, M. P., Kumar, S., and Tsai, M. D. (2007) A unified kinetic mechanism applicable to multiple DNA polymerases, Biochemistry 46, 5463-5472.
8. Beard, W. A., Shock, D. D., and Wilson, S. H. (2004) Influence of DNA structure on DNA polymerase beta active site function: Extension of mutagenic DNA intermediates, J. Biol. Chem. 279, 31921-31929.
9. Martinek, V., Bren, U., Goodman, M. F., Warshel, A., and Florián, J. (2007) DNA polymerase beta catalytic efficiency mirrors the Asn279-dCTP H-bonding strength, FEBS Lett. 581, 775-780.
10. Oelschlaeger, P. M. K. W. A. B. S. H. W. and Warshel, A. (2007) Magnesium-cationic dummy atom molecules enhance representation of DNA polymerase beta in molecular dynamics simulations: Improved accuracy in studies of structural features and mutational effects, J. Mol. Biol. 366, 687-701.
11. Lin, P., Pedersen, L. C., Batra, V. K., Beard, W. A., Wilson, S. H., and Pedersen, L. G. (2006) Energy analysis of chemistry for correct insertion by DNA polymerase beta, Proc. Natl. Acad. Sci. U.S.A. 103, 13294-13299.
12. Yang, L., Beard, W. A., Wilson, S. H., Broyde, S., and Schlick, T. (2002) Polymerase beta simulations suggest that Arg258 rotation is a slow step rather than large subdomain motions per se, J. Mol. Biol. 317, 679-699.
13. Beard, W. A., and Wilson, S. H. (1998) Structural insights into DNA polymerase beta fidelity: hold tight if you want it right, Chem. Biol. 5, R7-R13.
14. Hitomi, K., Iwai, S., and Tainer, J. A. (2007) The intricate structural chemistry of base excision repair machinery: Implications for DNA damage recognition, removal, and repair, DNA Repair 6, 410-428.
15. Lang, T. M., Maitra, M., Starcevic, D., Li, S. X., and Sweasy, J. B. (2004) A DNA polymerase beta mutant from colon cancer cells induces mutations, Proc. Natl. Acad. Sci. U.S.A. 101, 6074-6079.
16. Wang, L. M., Patel, U., Ghosh, L., and Banerjee, S. (1992) DNA polymerase beta mutations in human colorectal cancer, Cancer Res. 52, 4824-4827.
17. Sawaya, M. R., Prasad, R., Wilson, S. H., Kraut, J., and Pelletier, H. (1997) Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: Evidence for an induced fit mechanism, Biochemistry 36, 11205-11215.
18. Pelletier, H., Sawaya, M. R., Wolfle, W., Wilson, S. H., and Kraut, J. (1996) Crystal structures of human DNA polymerase β complexed with DNA: Implications for catalytic mechanism, processivity, and fidelity, Biochemistry 35, 12742-12761.
19. Arndt, J. W., Gong, W. M., Zhong, X. J., Showalter, A. K., Liu, J., Dunlap, C. A., Lin, Z., Paxson, C., Tsai, M. D., and Chan, M. K. (2001) Insight into the catalytic mechanism of DNA polymerase β: Structures of intermediate complexes, Biochemistry 40, 5368-5375.
20. Beard, W. A., and Wilson, S. H. (2006) Structure and mechanism of DNA polymerase β, Chem. Rev. 106, 361-382.
21. Krahn, J. M., Beard, W. A., and Wilson, S. H. (2004) Structural insights into DNA polymerase beta deterrents for misincorporation support an induced-fit mechanism for fidelity, Structure 12, 1823-1832.
22. Xiang, Y., Goodman, M. F., Beard, W. A., Wilson, S. H., and Warshel, A. (2007) Exploring the role of large conformational changes in the fidelity of DNA polymerase beta, Proteins 70, 231-247.
23. Florián, J., Goodman, M. F., and Warshel, A. (2005) Computer simulations of protein functions: Searching for the molecular origin of the replication fidelity of DNA polymerases, Proc. Natl. Acad. Sci. U.S.A. 102, 6819-6824.
24. Beard, W. A., and Wilson, S. H. (2003) Structural insights into the origins of DNA polymerase fidelity, Structure 11, 489-496.
25. Dunlap, C., and Tsai, M. D. (2002) Use of 2-aminopurine and tryptophan fluorescence as probes in kinetic analyses of DNA polymerase β, Biochemistry 41, 11226-11235.
26. Bose-Basu, B., DeRose, E. F., Kirby, T. W., Mueller, G. A., Beard, W. A., Wilson, S. H., and London, R. E. (2004) Dynamic characterization of a DNA repair enzyme: NMR studies of [methyl-C-13]methionine-labeled DNA polymerase β, Biochemistry 43, 8911-8922.
27. 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 beta, J. Biol. Chem. 278, 5072-5081.
28. Joyce, C. M., and Benkovic, S. J. (2004) DNA polymerase fidelity: Kinetics, structure, and checkpoints, Biochemistry 43, 14317-14324.
29. Showalter, A. K., and Tsai, M. D. (2002) A reexamination of the nucleotide incorporation fidelity of DNA polymerases, Biochemistry 41, 10571-10576.
30. Polesky, A. H., Dahlberg, M. E., Benkovic, S. J., Grindley, N. D. F., and Joyce, C. M. (1992) Side Chains Involved in Catalysis of the Polymerase Reaction of DNA Polymerase I from Escherichia coli, J. Biol. Chem. 267, 8417-8428.
31. Liu, J., and Tsai, M. D. (2001) DNA polymerase beta: Pre-steady-state kinetic analyses of dATPaS stereoselectivity and alteration of the stereoselectivity by various metal ions and by site-directed mutagenesis, Biochemistry 40, 9014-9022.
32. Hollfelder, F., and Herschlag, D. (1995) The nature of the transition state for enzyme-catalyzed phosphoryl transfer. Hydrolysis of O-aryl phosphorothioates by alkaline phosphatase, Biochemistry 34, 12255-12264.
33. Beard, W. A., and Wilson, S. H. (1995) Purification and domain-mapping of mammalian DNA polymerase beta, Methods Enzymol. 262, 98-107.
34. Upton, T. G., Osuna, J., Kashemirov, B. A., and McKenna, C. E. (2007) Synthesis of a series of methylene bisphosphonic acids and determination of stability constants by potentiometric titration. (In preparation).
35. Braun-Sand, S., Olsson, M. H. M., and Warshel, A. (2005) Computer modeling of enzyme catalysis and its relationship to concepts in physical organic chemistry, Adv. Phys. Org. Chem. 40, 201-245.
36. Warshel, A., Hwang, J. K., and Aqvist, J. (1992) Computer simulations of enzymatic reactions: Examination of linear free energy relationships and quantum mechanical corrections in the initial proton-transfer step of carbonic anhydrase, Faraday Discuss. 93, 225-238.
37. Albery, W. J. (1980) The application of the Marcus relation to reactions in solution, Annu. Rev. Phys. Chem. 31, 227-263.
38. Claessens, R. A. M. J., and Vanderlinden, J. G. M. (1984) Stability-constants of tin(II) and calcium diphosphonate complexes, J. Inorg. Biol. 21, 73-82.
39. Xiang, Y., Oelschlaeger, P., Florián, J., Goodman, M. F., and Warshel, A. (2006) Simulating the Effect of DNA Polymerase Mutations on Transition State Energetics and Fidelity: Evaluating Amino Acid Group Contribution and Allosteric Coupling for Ionized Residues in Human Pol β, Biochemistry 45, 7036-7048.
40. Florián, J., Goodman, M. F., and Warshel, A. (2002) Theoretical investigation of the binding free energies and key substrate-recognition components of the replication fidelity of human DNA polymerase β, J. Phys. Chem. B 106, 5739-5753.
41. Coxon, F. P., Thompson, K., and Rogers, M. J. (2006) Recent advances in understanding the mechanism of action of bisphosphonates, Curr. Opin. Pharmacol. 6, 307-312.
42. Fleisch, H. (2002) Development of bisphosphonates, Breast Cancer Res. 4, 30-34.
43. Castro, C., Smidansky, E., Maksimchuk, K. R., Arnold, J. J., Korneeva, V. S., Gotte, M., Konigsberg, W., and Cameron, C. E. (2007) Two proton transfers in the transition state for nucleotidyl transfer catalyzed by RNA- and DNA-dependent RNA and DNA polymerases, Proc. Natl. Acad. Sci. U.S.A. 104, 4267-4272.
44. Cleland, W. W. (1977) Determining the chemical mechanisms of enzyme-catalyzed reactions by kinetic studies, Adv. Enzymol. Relat. Areas Mol. Biol. 45, 273-387.
45. Hwang, J. K., and Warshel, A. (1996) How important are quantum mechanical nuclear motions in enzyme catalysis, J. Am. Chem. Soc. 118, 11745-11751.
46. Klahn, M., Rosta, E., and Warshel, A. (2006) On the mechanism of hydrolysis of phosphate monoesters dianions in solutions and proteins, J. Am. Chem. Soc. 128, 15310-15323.
47. Aqvist, J., Kolmodin, K., Florián, J., and Warshel, A. (1999) Mechanistic alternatives in phosphate monoester hydrolysis: What conclusions can be drawn from available experimental data, Chem. Biol. 6, R71-R80.
48. Kraynov, V. S., Showalter, A. K., Liu, J., Zhong, X. J., and Tsai, M. D. (2000) DNA polymerase β: Contributions of template-positioning and dNTP triphosphate-binding residues to catalysis and fidelity, Biochemistry 39, 16008-16015.
49. 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.
50. Mihai, C., Kravchuk, A. V., Tsai, M. D., and Bruzik, K. S. (2003) Application of Bronsted-type LFER in the study of the phospholipase C mechanism, J. Am. Chem. Soc. 125, 3236-3242.
51. Daniele, P. G., Rigano, C., and Sammartano, S. (1985) Ionic-strength dependence of formation-constants - Alkali-metal complexes of ethylenediaminetetraacetate, nitrolotriacetate, diphosphate, and tripolyphosphate in aqueous-solution, Anal. Chem. 57, 2956-2960.