DNA polymerase β catalytic efficiency mirrors the Asn279-dCTP H-bonding strength

FEBS Letters

Volumn 581, Issue 4, 2007, Pages 775-780

  Martínek, Václav ^a,b   Bren, Urban ^a,b   Goodman, Myron F ^c   Warshel, Arieh ^c   Florián, Jan ^a,b  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

DNA polymerase beta; dNTP; Enzyme preorganization; Free energy; Molecular dynamics; Near attack conformers; Site mutagenesis

Indexed keywords

ALANINE; ARGININE; ASPARAGINE; ASPARAGINE DERIVATIVE; DEOXYCYTIDINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE BETA; GLUTAMINE; GLYCINE; LYSINE; TYROSINE; VALINE;

ARTICLE; ATOM; CATALYSIS; CORRELATION COEFFICIENT; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; HYDROGEN BOND; INDUCED MUTATION; MOLECULAR DYNAMICS; MUTANT; PREDICTOR VARIABLE; PRIORITY JOURNAL; SIMULATION; WILD TYPE;

ASPARAGINE; BINDING SITES; CATALYSIS; DEOXYCYTOSINE NUCLEOTIDES; DNA POLYMERASE BETA; DNA PRIMERS; ELECTROSTATICS; HUMANS; HYDROGEN BONDING; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 33846807511     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2007.01.042     Document Type: Article

References (39)

1. Beard W.A., and Wilson S.H. Structure and mechanism of DNA polymerase β. Chem. Rev. 106 (2006) 361-382
2. Showalter A.K., Lamarche B.J., Bakhtina M., Su M.-I., Tang K.-H., and Tsai M.-D. Mechanistic comparison of high-fidelity and error-prone DNA polymerases and ligases involved in DNA repair. Chem. Rev. 106 (2006) 340-360
3. Srivastava D.K., Husain I., Arteaga C.L., and Wilson S.H. DNA polymerase beta expression differences in selected human tumors and cell lines. Carcinogenesis 20 (1999) 1049-1054
4. Dobashi Y., Kubota Y., Shuin T., Torigoe S., Yao M., and Hosaka M. Polymorphisms in the human DNA polymerase beta gene. Human Genet. 95 (1995) 389-390
5. Florián J., Goodman M.F., and Warshel A. Computer simulation of the chemical catalysis of DNA polymerases: discriminating between alternative nucleotide insertion mechanisms for T7 DNA polymerase. J. Am. Chem. Soc. 125 (2003) 8163-8177
6. Petruska, J., Goodman, M.F., Boosalis, M.S., Sowers, L.C., Cheong, C. and Tinoco Jr., I. (1988) Comparison between DNA melting thermodynamics and DNA polymerase fidelity. Proc. Natl. Acad. Sci. USA 85, 6252-6256.
7. Bren U., Martínek V., and Florián J. Free energy simulations of uncatalyzed DNA replication fidelity: structure and stability of T-G and dTTP-G terminal DNA mismatches flanked by a single dangling nucleotide. J. Phys. Chem. B 110 (2006) 10557-10566
8. Kraynov V.S., Showalter A.K., Liu J., Zhong X.J., and Tsai M.D. DNA polymerase β: contributions of template-positioning and dNTP triphosphate-binding residues to catalysis and fidelity. Biochemistry 39 (2000) 16008-16015
9. Kraynov V.S., Werneburg B.G., Zhong X., Lee H., Ahn J., and Tsai M.D. DNA polymerase β: analysis of the contributions of tyrosine-271 and asparagine-279 to substrate specificity and fidelity of DNA replication by pre-steady-state kinetics. Biochem. J. 323 (1997) 103-111
10. Ahn J., Werneburg B.G., and Tsai M.D. DNA polymerase β: structure-fidelity relationship from pre-steady-state kinetic analyses of all possible correct and incorrect base pairs for wild type and R283A mutant. Biochemistry 36 (1997) 1100-1107
11. Berg B.J.V., Beard W.A., and Wilson S.H. DNA structure and aspartate 276 influence nucleotide binding to human DNA polymerase beta - implication for the identity of the rate-limiting conformational change. J. Biol. Chem. 276 (2001) 3408-3416
12. Eyring H. The activated complex and the absolute rate of chemical reactions. Chem. Rev. 17 (1935) 65-77
13. Warshel A. Computer Modeling of Chemical Reactions in Enzymes and Solutions (1991), Wiley, New York
14. Doublie S., Sawaya M.R., and Ellenberger T. An open and closed case for all polymerases. Structure 7 (1999) R31-R35
15. Warshel A. Energetics of enzyme catalysis. Proc. Natl. Acad. Sci. USA 75 (1978) 5250
16. Xiang Y., Oelschlaeger P., Florián J., Goodman M.F., and Warshel A. 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 (2006) 7036-7048
17. Cornell W.D., et al. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117 (1995) 5179-5197
18. Marelius J., Kolmodin K., Feierberg I., and Åqvist J. Q: A molecular dynamics program for free energy calculations and empirical valence bond simulations in biomolecular systems. J. Mol. Graphics Model. 16 (1999) 213-225
19. Florián J., Goodman M.F., and Warshel A. 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 (2002) 5739-5753
20. Bren U., Martínek V., and Florián J. Decomposition of the solvation free energy of deoxyribonucleoside triphosphates using the free energy perturbation method. J. Phys. Chem. B 110 (2006) 12782-12788
21. King G., and Warshel A. A surface constrained all-atom solvent model for effective simulations of polar solutions. J. Chem. Phys. 91 (1989) 3647-3661
22. Lee F.S., and Warshel A. A local reaction field method for fast evaluation of long-range electrostatic interactions in molecular simulations. J. Chem. Phys. 97 (1992) 3100-3107
23. Alden R.G., Parson W.W., Chu Z.T., and Warshel A. Calculations of electrostatic energies in photosynthetic reaction centers. J. Am. Chem. Soc. 117 (1995) 12284-12298
24. Sham Y.Y., and Warshel A. The surface constraint all atom model provides size independent results in calculations of hydration free energies. J. Chem. Phys. 109 (1998) 7940-7944
25. Warshel A., Sharma P.K., Kato M., and Parson W.W. Modeling electrostatic effects in proteins. Biochim. Biophys. Acta 1764 (2006) 1647-1676
26. Humphrey W., Dalke A., and Schulten K. VMD - visual molecular dynamics. J. Mol. Graphics 14 1 (1996) 33-38
27. Batra V.K., Beard W.A., Shock D.D., Krahn J.M., Pedersen L.C., and Wilson S.H. Magnesium-induced assembly of a DNA polymerase catalytic complex. Structure 14 (2006) 1-10
28. McDonald I.K., and Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238 (1994) 777-793
29. Bruice T.C. A view at the millennium: the efficiency of enzymatic catalysis. Acc. Chem. Res. 35 (2002) 139-148
30. Beard W.A., et al. Enzyme-DNA interactions required for efficient nucleotide incorporation and discrimination in human DNA polymerase β. J. Biol. Chem. 271 (1996) 12141-12144
31. Lavrik O.I., et al. dNTP binding to HIV-1 reverse transcriptase and mammalian DNA polymerase β as revealed by affinity labeling with a photoreactive dNTP analog. J. Biol. Chem. 271 (1996) 21891-21897
32. Radhakrishnan R., Arora K., Wang Y., Beard W.A., Wilson S.H., and Schlick T. Regulation of DNA repair fidelity by molecular checkpoints: Gates in DNA polymerase β substrate selection. Biochemistry 45 (2006) 15142-15156
33. Showalter A.K., and Tsai M.D. A reexamination of the nucleotide incorporation fidelity of DNA polymerases. Biochemistry 41 (2002) 10571-10576
34. Bakhtina M., Lee S., Wang Y., Dunlap C., Lamarche B., and Tsai M.D. Use of viscogens, dNTPRS, and rhodium(III) as probes in stopped-flow experiments to obtain new evidence for the mechanism of catalysis by DNA polymerase. J. Am. Chem. Soc. 44 (2005) 5177-5187
35. Sucato C.A., et al. Modifying the β-γ leaving-group bridging oxygen alters nucleotide incorporation efficiency, fidelity and catalytic mechanism of DNA polymerase β. Biochemistry 46 (2007) 461-471
36. Warshel A. Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J. Biol. Chem. 273 (1998) 27035-27038
37. Cannon W.R., and Benkovic S.J. Solvation, reorganization energy, and biological catalysis. J. Biol. Chem. 273 (1998) 26257-26260
38. Beard W.A., Shock D.D., Yang X.P., DeLauder S.F., and Wilson S.H. Loss of DNA polymerase beta stacking interactions with templating purines, but not pyrimidines, alters catalytic efficiency and fidelity. J. Biol. Chem. 277 (2002) 8235-8242
39. Warshel A., and Florián J. Computer simulations of enzyme catalysis: finding out what has been optimized by evolution. Proc. Natl. Acad. Sci. USA 95 (1998) 5950-5955