Characterization of the Active Site of DNA Polymerase β by Molecular Dynamics and Quantum Chemical Calculation

Proteins: Structure, Function and Genetics

Volumn 53, Issue 3, 2003, Pages 667-682

  Rittenhouse, Robert C ^a   Apostoluk, Wlodzimierz K ^a   Miller, John H ^a   Straatsma, T P ^a  

^a PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

Coordination; Geometry optimization; Hydrogen bond; Magnesium complex; Metalloenzyme; Molecular dynamics; Quantum calculation; Tightly bound water

Indexed keywords

DNA; DNA DIRECTED DNA POLYMERASE BETA; MAGNESIUM ION; METALLOPROTEINASE; NUCLEOSIDE TRIPHOSPHATE; WATER;

AB INITIO CALCULATION; ARTICLE; CALCULATION; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STRUCTURE; HYDROGEN BOND; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM CHEMISTRY;

BINDING SITES; CATALYSIS; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; DNA POLYMERASE BETA; HYDROGEN BONDING; LIGANDS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTONS; QUANTUM THEORY; WATER;

EID: 0242267522     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.10451     Document Type: Article

References (45)

1. Lindahl T, Wood RD. Quality control by DNA repair. Science 1999;286:1897-1905.
2. Aaltonen LA, Peltomaki P, Leach FS, Sistonen P, Pylkkanen L, Mecklin JP, Jarvinen H, Powell SM, Jen J, Hamilton SR, Perersen GM, Kinzler KW, Vogelstein B, Delachapelle A. Clues to the pathogenesis of familial colorectal cancer. Science 1993;260:812-816.
3. Loeb LA, Christians FC. Multiple mutations in human cancers. Mutation Res 1996;350:279-286.
4. Friedberg EC, Walker GC, Siede W. DNA repair and mutagenesis. New York: ASM Press; 1995.
5. Seeberg E, Eide L, Bjoras M. The base excision repair pathway. Trends Biochem Sci 1995;20:391-397.
6. Sobol RW, Horton JK, Kuhn R, Gu H, Singhal RK, Prasad R, Rajewsky K, Wilson SH. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 1996;379:183-186.
7. Matsumoto Y, Kim K. Excision of deoxyribose phosphate residues by DNA polymerase beta during DNA repair. Science 1995;269:699-702.
8. Brautigam CA, Steitz TA. Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr Opin Struc Biol 1998;8:54-63.
9. Sawaya MR, Prasad R, Wilson SH, Kraut J, Pelletier H. Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: Evidence for an induced fit mechanism. Biochemistry 1997;36:11205-11215.
10. Arndt JW, Gong W, Zhong X, Showalter AK, Liu J, Dunlap CA, Lin Z, Paxson C, Tsai MD, Chan MK. Insight into the catalytic mechanism of DNA polymerase beta: Structures of intermediate complexes. Biochemistry 2001;40:5368-5375.
11. Werneburg BG, Ahn J, Zhong X, Hondal RJ, Kraynov VS, Tsai MD. DNA polymerase beta: Pre-steady-state kinetic analysis and roles of arginine-283 in catalysis and fidelity. Biochemistry 1996;35:7041-7050.
12. Zhong X, Patel SS, Werneburg BG, Tsai MD. DNA polymerase beta: Multiple conformational changes in the mechanism of catalysis. Biochemistry 1997;36:11891-11900.
13. Pelletier H, Sawaya MR, Wolfe W, Wilson SH, Kraut J. Crystal structures of human DNA polymerase beta complexed with DNA: Implications for catalytic mechanism, processivity, and fidelity. Biochemistry 1996;35:12742-12761.
14. Pelletier H, Sawaya MR, Wolfe W, Wilson SH, Kraut J. A structural basis for metal ion mutagenicity and nucleotide selectivity in human DNA polymerase beta. Biochemistry 1996;35:12762-12777.
15. Opresko L, Shiman R, Eckert KA. Hydrophobic interactions in the hinge domain of DNA polymerase beta are important but not sufficient for maintaining fidelity of DNA synthesis. Biochemistry 2000;39:11399-11407.
16. Pelletier H, Sawaya MR, Kumar A, Wilson SH, Kraut J. Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP. Science 1994;264:1891-1903.
17. Yang L, Beard WA, Wilson SH, Broyde S, Schlick T. Polymerase beta simulations suggest that Arg258 rotation is a slow step rather than large subdomain motions per se. J Mol Biol 2002;317:651-671.
18. Showalter AK, Ming-Daw T. A reexamination of the nucleotide incorporation fidelity of DNA polymerases. Biochemistry 2002;41:10571-10576.
19. Doublie S, Tabor S, Long AM, Richardson CC, Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 1998;391:251-258.
20. Kiefer JR, Mao C, Braman JC, Beese LS. Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal. Nature 1998;391:304-307.
21. Steitz TA. A mechanism for all polymerases. Nature 1998;391:231-232.
22. Dudev T, Cowan JA, Lim C. Competitive binding in magnesium coordination chemistry: Water versus ligands of biological interest. J Am Chem Soc 1999;121:7665-7673.
23. Larsen TM, Wedekind JE, Rayment I, Reed, GH. A carboxylate oxygen of the substrate bridges the magnesium ions at the active site of enolase: Structure of the yeast enzyme complexed with the equilibrium mixture of 2-phosphoglycerate and phosphoenolpyruvate at 1.8 Å resolution. Biochemistry 1996;35:4349-4358.
24. Bock CW, Katz AK, Glusker JP. Hydration of zinc ions-a comparison with magnesium and beryllium ions. J Am Chem Soc 1995;117:3754-3763.
25. Bernstein FC, Koetzle TF, Williams GJ, Meyer EF Jr, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M. The Protein Data Bank: A computer-based archival file for macromolecular structures. J Mol Biol 1977;112:535-542.
26. Oda Y, Yamazaki T, Nagayama K, Kanaya S, Kuroda Y, Nakamura H. Individual ionization constants of all the carboxyl groups in ribonuclease HI from Escherichia coli determined by NMR. Biochemistry 1994;33:5275-5284.
27. Straatsma TP, Apra E, Windus TL, Dupuis M, Bylaska EJ, De Jong WA, Hirata S, Smith DMA, Hackler MT, Pollack L, Harrison RJ, Nieplocha J, Tipparaju V, Krishnan M, Brown E, Cisneros G, Fann GI, Fruchtl H, Garza J, Hirao K, Kendall RA, Nichols JA, Tsemekhman K, Valiev M, Wolinski K, Anchell J, Bernholdt D, Borowski P, Clark T, Clerc D, Dachsel H, Deegan M, Dyall K, Elwood D, Glendening E, Gutowski M, Hess A, Jaffe J, Johnson B, Ju J, Kobayashi R, Kutteh R, Lin Z, Littlefield R, Long X, Meng B, Nakajima T, Niu S, Rosing M, Sandrone G, Stave M, Taylor H, Thomas G, Van Lenthe J, Wong A, Zhang Z. "NWChem, a computational chemistry package for parallel computers. Version 4.5" Pacific Northwest National Laboratory, Richland WA, 2003.
28. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. A second generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules. J Am Chem Soc 1995;117:5179-5197.
29. Åqvist J. Ion water interaction potentials derived from free-energy perturbation simulations. J Phys Chem 1990;94:8021-8024.
30. Bayly CI, Cieplak P, Cornell WD, Kollman PA. A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges-the RESP model. J Phys Chem 1993;97:10269-10280.
31. Berendsen HJC, Grigera JR, Straatsma TP. The missing term in effective pair potentials. J Phys Chem 1987;91:6269-6271.
32. Berendsen HJC, Postma JPM, van Gunsteren WF, Dinola A, Haak JR. Molecular-dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
33. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG. A smooth particle mesh Ewald method. J Chem Phys 1995;103:8577-8593.
34. Ryckaert JP, Ciccotti G., Berendsen HJC. Numerical integration of Cartesian equations of motion of a system with constrains: Molecular dynamics of n-alkanes. J Comp Phys 1977;23:327-341.
35. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Zakrzewski VG, Montgomery, Jr. JA, Stratmann RE, Burant JC, Dapprich S, Millam JM, Daniels AD, Kudin KN, Strain MC, Farkas O, Tomasi J, Barone V, Cossi M, Cammi R, Mennucci B, Pomelli C, Adamo C, Clifford S, Ochterski J, Petersson GA, Ayala PY, Cui Q, Morokuma K, Rega N, Salvador P, Dannenberg JJ, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Cioslowski J, Ortiz JV, Baboul AG, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Gomperts R, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Andres JL, Gonzalez C, Head-Gordon M, Replogle ES, Pople JA. Gaussian 98, Revision A. 11.3. Gaussian, Inc., Pittsburgh PA, 2002.
36. Zhan C-G, de Souza ON, Rittenhouse RC, Ornstein RL. Determination of two structural forms of catalytic bridging ligand in zinc-phosphotriesterase by molecular dynamics simulation and quantum chemical calculation. J Am Chem Soc 1999;121:7279-7282.
37. Diaz N, Suarez D, Merz KM. Zinc metallo-beta-lactamase from Bacteroides fragilis: A quantum chemical study on model systems of the active site. J Am Chem Soc 2000;122:4197-4208.
38. Koca J, Zhan C-G, Rittenhouse RC, Ornstein RL. Mobility of the active site bound paraoxon and sarin in zinc-phosphotriesterase by molecular dynamics simulation and quantum chemical calculation. J Am Chem Soc 2001;123:817-826.
39. Glendening ED, Feller D. Dication-water interactions: M(2+)(H2O)(n) clusters for alkaline earth metals M = Mg, Ca, Sr, Ba, and Ra. J Phys Chem 1996;100:4790-4797.
40. Pavlov M, Siegbahn EM, Sandstrom M. Hydration of beryllium, magnesium, calcium, and zinc ions using density functional theory. J Phys Chem A 1998;102:219-228.
41. Stryer L. Biochemistry. New York: Freeman; 1988.
42. Abashkin YG, Erickson JW, Burt SK. Quantum chemical investigation of enzymatic activity in DNA polymerase beta: A mechanistic study. J Phys Chem B 2001;105:287-292.
43. Garmer DR, Gresh N. A comprehensive energy component analysis of the interaction of hard and soft dications with biological ligands. J Am Chem Soc 1994;116:3556-3567.
44. Allen FH, Bellard S, Brice MD, Cartwright BA, Doubleday A., Higgs H, Hummelink T, Hummelink-Peters BG, Kennard O, Motherwell WDS, Rodgers JR, Watson DG. The Cambridge Crystallographic Data Centre: Computer-based search, retrieval, analysis and display of information. Acta Crystallogr 1979;B35:2331-2339.
45. Alberts IL, Nadassy K, Wodak SJ. Analysis of zinc binding sites in protein crystal structures. Protein Sci 1998;7:1700-1716.