A unified kinetic mechanism applicable to multiple DNA polymerases

Biochemistry

Volumn 46, Issue 18, 2007, Pages 5463-5472

  Bakhtina, Marina ^a   Roettger, Michelle P ^a   Kumar, Sandeep ^a   Tsai, Ming Daw ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b GENOMICS RESEARCH CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; CONFORMATIONS; DNA; FLUORESCENCE; NUCLEOTIDES; VISCOSITY;

DNA POLYMERASE; FLUORESCENCE TRANSITION; KLENOW FRAGMENT (KF);

ENZYME KINETICS;

DNA DIRECTED DNA POLYMERASE BETA; DNA POLYMERASE;

AFRICAN SWINE FEVER VIRUS; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; KINETICS; MAMMAL; MUTANT; NONHUMAN; PH; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; VISCOSITY;

AFRICAN SWINE FEVER VIRUS; ALANINE; ANIMALS; ARGININE; CATALYSIS; DNA POLYMERASE I; DNA-DIRECTED DNA POLYMERASE; KINETICS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RATS;

AFRICAN SWINE FEVER VIRUS; MAMMALIA;

EID: 34248370198     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700084w     Document Type: Article

References (43)

1. Showalter, A. K., Lamarche, B. J., Bakhtina, M., Su, M. I., Tang, K. H., and Tsai, M. D. (2006) Mechanistic comparison of high-fidelity and error-prone DNA polymerases and ligases involved in DNA repair, Chem. Rev. 106, 340-60.
2. Kuchta, R. D., Mizrahi, V., Benkovic, P. A., Johnson, K. A., and Benkovic, S. J. (1987) Kinetic mechanism of DNA polymerase I (Klenow), Biochemistry 26, 8410-17.
3. Patel, S. S., Wong, I., and Johnson, K. A. (1991) Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant, Biochemistry 30, 511-25.
4. Dahlberg, M. E., and Benkovic, S. J. (1991) Kinetic mechanism of DNA polymerase I (Klenow fragment): identification of a second conformational change and evaluation of the internal equilibrium constant, Biochemistry 30, 4835-43.
5. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity, Annu. Rev. Biochem. 62, 685-713.
6. Doublie, S., Sawaya, M. R., and Ellenberger, T. (1999) An open and closed case for all polymerases, Structure 7, R31-R35.
7. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity, Annu. Rev. Biochem. 69, 497-529.
8. Sawaya, M. R., Prasad, R., Wilson, S. H., Kraut, J., and 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.
9. Arndt, J. W., Gong, W., Zhong, X., 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.
10. Dunlap, C. A., 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.
11. Showalter, A. K., and Tsai, M.-D. (2002) A Reexamination of the Nucleotide Incorporation Fidelity of DNA Polymerases, Biochemistry 41, 10571-10576.
12. 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.
13. Rothwell, P. J., Mitaksov, V., and Waksman, G. (2005) Motions of the fingers subdomain of Klentaql are fast and not rate limiting: Implications for the molecular basis of fidelity in DNA polymerases, Mol. Cell 19, 345-355.
14. 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.
15. Arora, K., Beard, W. A., Wilson, S. H., and Schlick, T. (2005) Mismatch-Induced Conformational Distortions in Polymerase β Support an Induced-Fit Mechanism for Fidelity, Biochemistry 44, 13328-13341.
16. Joyce, C. M., and Benkovic, S. J. (2004) DNA polymerase fidelity: Kinetics, structure, and checkpoints, Biochemistry 43, 14317-14324.
17. Purohit, V., Grindley, N. D. F., and Joyce, C. M. (2003) Use of 2-Aminopurine Fluorescence To Examine Conformational Changes during Nucleotide Incorporation by DNA Polymerase I (Klenow Fragment), Biochemistry 42, 10200-10211.
18. 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.
19. Kunkel, T. A. (2004) DNA Replication Fidelity, J. Biol. Chem. 279, 16895-16898.
20. Zhong, X., Patel, S. S., and Tsai, M.-D. (1998) DNA Polymerase β. 5. Dissecting the Functional Roles of the Two Metal Ions with Cr(III)dTTP, J. Am. Chem. Soc. 120, 235-236.
21. Zhong, X., Patel, S. S., Werneburg, B. G., and Tsai, M.-D. (1997) DNA polymerase β: Multiple conformational changes in the mechanism of catalysis, Biochemistry 36, 11891-11900.
22. Bakhtina, M., Lee, S., Wang, Y., Dunlap, C. A., Lamarche, B. J., and Tsai, M.-D. (2005) Use of Viscogens, dNTPαS, 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.
23. Gavish, B., and Werber, M. M. (1979) Viscosity-dependent structural fluctuations in enzyme catalysis, Biochemistry 18, 1269-75.
24. Kanosue, Y., Kojima, S., and Ohkata, K. (2004) Influence of solvent viscosity on the rate of hydrolysis of dipeptides by carboxypeptidase Y, J. Phys. Org. Chem. 17, 448-457.
25. Radhakrishnan, R., and Schlick, T. (2004) 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. U.S.A. 101, 5970-5975.
26. 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, 651-671.
27. 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.
28. Werneburg, B. G., Ahn, J., Zhong, X., Hondal, R. J., Kraynov, V. S., and Tsai, M.-D. (1996) DNA Polymerase β: Pre-Steady-State Kinetic Analysis and Roles of Arginine-283 in Catalysis and Fidelity, Biochemistry 35, 7041-7050.
29. Showalter, A. K., and Tsai, M.-D. (2001) A DNA Polymerase with Specificity for Five Base Pairs, J. Am. Chem. Soc. 123, 1776-1777.
30. Joyce, C. M., and Derbyshire, V. (1995) Purification of Escherichia coli DNA polymerase I and Klenow fragment, Methods Enzymol. 262, 3-13.
31. Frey, M. W., Sowers, L. C., Millar, D. P., and Benkovic, S. J. (1995) The nucleotide analog 2-aminopurine as a spectroscopic probe of nucleotide incorporation by the Klenow fragment of Escherichia coli polymerase I and bacteriophage T4 DNA polymerase, Biochemistry 34, 9185-92.
32. Menge, K. L., Hostomsky, Z., Nodes, B. R., Hudson, G. O., Rahmati, S., Moomaw, E. W., Almassy, R. J., and Hostomska, Z. (1995) 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, 15934-42.
33. Maciejewski, M. W., Shin, R., Pan, B., Marintchev, A., Denninger, A., Mullen, M. A., Chen, K., Gryk, M. R., and Mullen, G. P. (2001) Solution structure of a viral DNA repair polymerase, Nat. Struct. Biol. 8, 936-941.
34. Showalter, A. K., Byeon, I.-J. L., Su, M.-I., and Tsai, M.-D. (2001) Solution structure of a viral DNA polymerase X and evidence for a mutagenic function, Nat. Struct. Biol. 8, 942-946.
35. Yin, Y. W., and Steitz, T. A. (2004) The structural mechanism of translocation and helicase activity in T7 RNA polymerase, Cell 116, 393-404.
36. Ahn, J., Werneburg, B. G., and Tsai, M.-D. (1997) 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, 1100-1107.
37. Kraynov, V. S., Werneburg, B. G., Zhong, X., Lee, H., Ahn, J., and Tsai, M. D. (1997) 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 (Part 1), 103-11.
38. Tsai, Y.-C., and Johnson, K. A. (2006) A New Paradigm for DNA Polymerase Specificity, Biochemistry 45, 9675-9687.
39. Herschlag, D., Piccirilli, J. A., and Cech, T. R. (1991) Ribozyme-catalyzed and nonenzymic reactions of phosphate diesters: rate effects upon substitution of sulfur for a nonbridging phosphoryl oxygen atom, Biochemistry 30, 4844-54.
40. Liu, J., and Tsai, M. D. (2001) DNA polymerase β: pre-steady-state kinetic analyses of dATPαS stereoselectivity and alteration of the stereoselectivity by various metal ions and by site-directed mutagenesis, Biochemistry 40, 9014-22.
41. Benitez, B. A. S., Arora, K., and Schlick, T. (2006) In silico studies of the African swine fever virus DNA polymerase X support an induced-fit mechanism, Biophys. J. 90, 42-56.
42. 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 β, Proc. Natl. Acad. Sci. U.S.A. 103, 13294-13299.
43. Xiang, Y., Oelschlaeger, P., Florian, 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.