Magnesium-cationic Dummy Atom Molecules Enhance Representation of DNA Polymerase β in Molecular Dynamics Simulations: Improved Accuracy in Studies of Structural Features and Mutational Effects

Journal of Molecular Biology

Volumn 366, Issue 2, 2007, Pages 687-701

  Oelschlaeger, Peter ^a   Klahn, Marco ^a   Beard, William A ^b   Wilson, Samuel H ^b   Warshel, Arieh ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

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

Author keywords

DNA polymerase; magnesium ion; metalloenzyme; molecular dynamics; mutation

Indexed keywords

CATION; DNA DIRECTED DNA POLYMERASE BETA; MAGNESIUM ION;

ARTICLE; ATOM; ENERGY TRANSFER; ENZYME STRUCTURE; EXPERIMENTAL STUDY; FORCE; HUMAN; MICHAELIS CONSTANT; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR MODEL; MUTATIONAL ANALYSIS; PHASE TRANSITION; PRIORITY JOURNAL; SIMULATION;

EID: 84962408666     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.095     Document Type: Article

References (43)

1. Kornberg A., and Baker T.A. DNA Replication (1992), W. H. Freeman, New York
2. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., and Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004) 39-85
3. Rothwell P.J., and Waksman G. Structure and mechanism of DNA polymerases. Advan. Protein Chem. 71 (2005) 401-440
4. Beard W.A., and Wilson S.H. Structure and mechanism of DNA polymerase β. Chem. Rev. 106 (2006) 361-382
5. Wiebauer K., and Jiricny J. Mismatch-specific thymine DNA glycosylase and DNA polymerase β mediate the correction of G.T mispairs in nuclear extracts from human cells. Proc. Natl Acad. Sci. USA 87 (1990) 5842-5845
6. 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
7. Sawaya M.R., Pelletier H., Kumar A., Wilson S.H., and Kraut J. Crystal structure of rat DNA polymerase β: evidence for a common polymerase mechanism. Science 264 (1994) 1930
8. Sawaya M.R., Prasad R., Wilson S.H., Kraut J., and Pelletier H. Crystal structures of human DNA polymerase β complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 36 (1997) 11205-11215
9. Batra V.K., Beard W.A., Shock D.D., Krahn J.M., Pedersen L.C., and Wilson S.H. Magnesium-induced assembly of a complete DNA polymerase catalytic complex. Structure 14 (2006) 757-766
10. Fothergill M., Goodman M.F., Petruska J., and Warshel A. Structure-energy analysis of the role of metal ions in phosphodiester bond hydrolysis by DNA polymerase I. J. Am. Chem. Soc. 117 (1995) 11619-11627
11. Radhakrishnan R., and Schlick T. Orchestration of cooperative events in DNA synthesis and repair mechanism unraveled by transition path sampling of DNA polymerase β's closing. Proc. Natl Acad. Sci. USA 101 (2004) 5970-5975
12. Yang L.J., Beard W.A., Wilson S.H., Broyde S., and Schlick T. 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 (2004) 3392-3408
13. Florian J., Goodman M.F., and Warshel A. Computer simulation studies of the fidelity of DNA polymerases. Biopolymers 68 (2003) 286-299
14. Florian J., Goodman M.F., and Warshel A. Computer simulations of protein functions: Searching for the molecular origin of the replication fidelity of DNA polymerases. Proc. Natl Acad. Sci. USA 102 (2005) 6819-6824
15. Florian 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
16. Xiang Y., Oelschlaeger P., Florian 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. Shurki A., and Warshel A. Structure/function correlations of protreins using MM, QM/MM and related approaches; methods, concepts, pitfalls and current progress. Advan. Protein Chem. 66 (2003) 249-312
18. Åqvist J. Ion-water interaction potentials derived from free energy perturbation simulations. J. Chem. Phys. 94 (1990) 8021-8024
19. Stote R.H., and Karplus M. Zinc binding in proteins and solution: a simple but accurate nonbonded representation. Proteins: Struct. Funct. Genet. 23 (1995) 12-31
20. Hoops S.C., Anderson K.W., and Merz K.M. Force field design for metalloproteins. J. Am. Chem. Soc. 113 (1991) 8262
21. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz Jr. K.M., Ferguson D.M., 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
22. Lee F.S., Chu Z.T., and Warshel A. Microscopic and semimicroscopic calculations of electrostatic energies in proteins by the POLARIS and ENZYMIX programs. J. Comput. Chem. 14 (1993) 161-185
23. Åqvist J., and Warshel A. Free-energy relationships in metalloenzyme-catalyzed reactions - calculations of the effects of metal-ion substitutions in staphylococcal nuclease. J. Am. Chem. Soc. 112 (1990) 2860-2868
24. Åqvist J., and Warshel A. Computer simulation of the initial proton transfer step in human carbonic anhydrase I. J. Mol. Biol. 224 (1992) 7-14
25. Pang Y.P., Xu K., Yazal J.E., and Prendergast F.G. Successful molecular dynamics simulation of the zinc-bound farnesyltransferase using the cationic dummy atom approach. Protein Sci. 9 (2000) 1857-1865
26. Park J.G., Sill P.C., Makiyi E.F., Garcia-Sosa A.T., Millard C.B., Schmidt J.J., and Pang Y.P. Serotype-selective, small-molecule inhibitors of the zinc endopeptidase of botulinum neurotoxin serotype A. Bioorg. Med. Chem. 14 (2006) 395-408
27. Pang Y.P. Successful molecular dynamics simulation of two zinc complexes bridged by a hydroxide in phosphotriesterase using the cationic dummy atom method. Proteins: Struct. Funct. Genet. 45 (2001) 183-189
28. Oelschlaeger P., Schmid R.D., and Pleiss J. Insight into the mechanism of the IMP-1 metallo-β-lactamase by molecular dynamics simulations. Protein Eng. 16 (2003) 341-350
29. Oelschlaeger P., Schmid R.D., and Pleiss J. Modeling domino effects in enzymes: molecular basis of the substrate specificity of the bacterial metallo-β-lactamases IMP-1 and IMP-6. Biochemistry 42 (2003) 8945-8956
30. Kubo R., Toda M., and Hashitsume N. Statistical Physics II: Nonequilibrium Statistical Mechanics (1985), Springer-Verlag, Berlin
31. Hwang J.-K., and Warshel A. Microscopic examination of free energy relationships for electron transfer in polar solvents. J. Am. Chem. Soc. 109 (1987) 715-720
32. Schutz C.N., and Warshel A. What are the dielectric "constants" of proteins and how to validate electrostatic models. Proteins: Struct. Funct. Genet. 44 (2001) 400-417
33. Arndt J.W., Gong W.M., Zhong X.J., Showalter A.K., Liu J., Dunlap C.A., et al. Insight into the catalytic mechanism of DNA polymerase β: structures of intermediate complexes. Biochemistry 40 (2001) 5368-5375
34. Noyes R.M. Thermodynamics of ion hydration as a measure of effective dielectric properties of water. J. Am. Chem. Soc. 84 (1962) 513-522
35. Pavlov M., Siegbahn P.E.M., and Sandstrom M. Hydration of beryllium, magnesium, calcium, and zinc ions using density functional theory. J. Phys. Chem. A 102 (1998) 219-228
36. Warshel A., Sussman F., and King G. Free energy of charges in solvated proteins: microscopic calculations using a reversible charging process. Biochemistry 25 (1986) 8368-8372
37. Warshel A. Computer Modeling of Chemical Reactions in Enzymes and Solutions (1991), John Wiley & Sons, New York
38. Miertus S., Scrocco E., and Tomasi J. Electrostatic interaction of a solute with a continuum. A direct utilization of ab initio molecular potentials for the prevision of solvent effects. J. Chem. Phys. 55 (1981) 117-129
39. Harding M.M. Geometry of metal-ligand interactions in proteins. Acta Crystallog. sect. D 57 (2001) 401-411
40. 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
41. Menge K.L., Hostomsky Z., Nodes B.R., Hudson G.O., Rahmati S., Moomaw E.W., et al. Structure-function analysis of the mammalian DNA polymerase β active site: role of aspartic acid 256, arginine 254, and arginine 258 in nucleotidyl transfer. Biochemistry 34 (1995) 15934-15942
42. Lee F.S., Chu Z.T., Bolger M.B., and Warshel A. Calculations of antibody-antigen interactions: microscopic and semi-microscopic evaluation of the free energies of binding of phosphorylcholine analogs to McPC603. Protein Eng. 5 (1992) 215-228
43. Humphrey W., Dalke A., and Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996) 33-38