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

Volumn 44, Issue 13, 2005, Pages 5177-5187

  Bakhtina, Marina ^a   Lee, Soojin ^a   Wang, Yu ^a   Dunlap, Chris ^a   Lamarche, Brandon ^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

CATALYSIS; COMPUTATIONAL METHODS; CONFORMATIONS; DNA; ENZYMES; FLUORESCENCE; GLUCOSE; SUGAR (SUCROSE); VISCOSITY;

CONFORMATIONAL CHANGE; FLUORESCENCE TRASITION SELECTIVITY; KINETIC MECHANISM; POLYMERASE;

RHODIUM;

2' DEOXYNUCLEOSIDE 5' O (1 THIOTRIPHOSPHATE); DNA DIRECTED DNA POLYMERASE BETA; MAGNESIUM; NUCLEOSIDE TRIPHOSPHATE; RHODIUM; UNCLASSIFIED DRUG; DEOXYRIBONUCLEOTIDE; DNA; NUCLEOTIDE; RECOMBINANT PROTEIN; TRYPTOPHAN;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STRUCTURE; FLUORESCENCE; METAL BINDING; METHODOLOGY; PRIORITY JOURNAL; STOPPED FLOW METHOD; VISCOSITY; ANIMAL; CHEMISTRY; ENZYME SPECIFICITY; IN VITRO STUDY; KINETICS; METABOLISM; MOLECULAR PROBE; NUCLEOTIDE SEQUENCE; RAT; SPECTROFLUOROMETRY;

ANIMALS; BASE SEQUENCE; CATALYSIS; DEOXYRIBONUCLEOTIDES; DNA; DNA POLYMERASE BETA; KINETICS; MAGNESIUM; MOLECULAR PROBES; RATS; RECOMBINANT PROTEINS; RHODIUM; SPECTROMETRY, FLUORESCENCE; SUBSTRATE SPECIFICITY; THIONUCLEOTIDES; TRYPTOPHAN; VISCOSITY;

EID: 16344376908     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047664w     Document Type: Article

References (50)

1. 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.
2. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity, Annu. Rev. Biochem. 69, 497-529.
3. Showalter, A. K., and Tsai, M.-D. (2002) A Reexamination of the Nucleotide Incorporation Fidelity of DNA Polymerases, Biochemistry 41, 10571-10576.
4. Kunkel, T. A. (2004) DNA Replication Fidelity, J. Biol. Chem. 279, 16895-16898.
5. 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.
6. 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.
7. 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, 9014-9022.
8. 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.
9. 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.
10. Pelletier, H., Sawaya, M. R., Kumar, A., Wilson, S. H., and Kraut, J. (1994) Structures of ternary complexes of rat DNA polymerase β, a DNA template-primer, and ddCTP, Science (Washington, D.C.) 264, 1891-903.
11. Pelletier, H., Sawaya, M. R., Woffle, 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.
12. Sawaya, M. R., Pelletier, H., Kumar, A., Wilson, S. H., and Kraut, J. (1994) Crystal structure of rat DNA polymerase β: evidence for a common polymerase mechanism, Science (Washington, D.C.) 264, 1930-1935.
13. 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.
14. 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.
15. 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.
16. 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.
17. Fiala, K. A., and Suo, Z. (2004) Mechanism of DNA Polymerization Catalyzed by Sulfolobus solfataricus P2 DNA Polymerase IV, Biochemistry 43, 2116-2125.
18. Gohara, D. W., Arnold, J. J., and Cameron, C. E. (2004) Poliovirus RNA-Dependent RNA Polymerase (3Dpol): Kinetic, Thermodynamic, and Structural Analysis of Ribonucleotide Selection, Biochemistry 43, 5149-5158.
19. 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.
20. 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.
21. 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.
22. 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.
23. Warshaw, M. M., and Cantor, C. R. (1970) Oligonucleotide interactions. IV. Conformational differences between deoxy- and ribodinucleoside phosphates, Biopolymers 9, 1079-103.
24. Lu, Z., Shorter, A. L., Lin, I., and Dunaway-Mariano, D. (1988) Preparation and configurational analysis of the stereoisomers of b,g-bidentate Rh(H2O)4ATP and a,b,g-tridentate Rh(H2O)3ATP. A new class of enzyme active site probes, Inorg. Chem. 27,4135-4139.
25. Ayres, G. H., and Forrester, J. S. (1957) Preparation of rhodium-(III) perchlorate hexahydrate, J. Inorg. Nucl. Chem. 3, 365-366.
26. Cole, P. A., Burn, P., Takacs, B., and Walsh, C. T. (1994) Evaluation of the catalytic mechanism of recombinant human Csk (C-terminal Src kinase) using nucleotide analogs and viscosity effects, J. Biol. Chem. 269, 30880-30887.
27. 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.
28. Kurz, L. C., Weitkamp, E., and Frieden, C. (1987) Adenosine deaminase: viscosity studies and the mechanism of binding of substrate and of ground- and transition-state analog inhibitors, Biochemistry 26, 3027-3032.
29. Lew, J., Taylor, S. S., and Adams, J. A. (1997) Identification of a partially rate-determining step in the catalytic mechanism of cAMP-dependent protein kinase: A transient kinetic study using stopped-flow fluorescence spectroscopy, Biochemistry 36, 6717-6724.
30. Shaffer, J., Sun, G., and Adams, J. A. (2001) Nucleotide Release and Associated Conformational Changes Regulate Function in the COOH-Terminal Src Kinase, Csk, Biochemistry 40, 11149-11155.
31. Gavish, B., and Werber, M. M. (1979) Viscosity-dependent structural fluctuations in enzyme catalysis, Biochemistry 18, 1269-1275.
32. Arnold, J. J., and Cameron, C. E. (2004) Poliovirus RNA-Dependent RNA Polymerase (3Dpol): Pre-Steady-State Kinetic Analysis of Ribonucleotide Incorporation in the Presence of Mg2+, Biochemistry 43, 5126-5137.
33. Einolf, H. J., and Guengerich, F. P. (2001) Fidelity of nucleotide insertion at 8-oxo-7,8-dihydroguanine by mammalian DNA polymerase d: steady-state and pre-steady-state kinetic analysis, J. Biol. Chem. 276, 3764-3771.
34. Kuchta, R. D., Benkovic, P., and Benkovic, S. J. (1988) Kinetic mechanism whereby DNA polymerase I (Klenow) replicates DNA with high fidelity, Biochemistry 27, 6716-6725.
35. 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, 511-525.
36. Washington, M. T., Prakash, L., and Prakash, S. (2001) Yeast DNA polymerase h utilizes an induced-fit mechanism of nucleotide incorporation, Cell (Cambridge, Mass.) 107, 917-927.
37. 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, 9185-9192.
38. Joyce, C. M., and Steitz, T. A. (1994) Function and structure relationships in DNA polymerases, Annu. Rev. Biochem. 63, 777-822.
39. Steitz, T. A. (1999) DNA polymerases: structural diversity and common mechanisms, J. Biol. Chem. 274, 17395-17398.
40. Cowan, J. A. (1998) Metal Activation of Enzymes in Nucleic Acid Biochemistry, Chem. Rev. (Washington, D.C.) 98, 1067-1087.
41. Cleland, W. W. (1982) Preparation of chromium(III) and cobalt-(III) nucleotides as chirality probes and inhibitors, Methods Enzymol. 87, 159-179.
42. Kuntzweiler, T. A., and Grisham, C. M. (1992) Inactivation and phosphorylation of sacroplasmic reticulum calcium-ATPase by magnesium. ATP analogs rhodium(III)-ATP and cobalt(III)-ATP, Arch. Biochem. Biophys. 295, 188-197.
43. Lu, Z., Shorter, A. L., and Dunaway-Mariano, D. (1993) Investigations of kinase substrate specificity with aqua rhodium(III) complexes of adenosine 5′-triphosphate, Biochemistry 32, 2378-2385.
44. Pappu, K. M., Kunnumal, B., and Serpersu, E. H. (1997) A new metal-binding site for yeast phosphoglycerate kinase as determined by the use of a metal-ATP analog, Biophys. J. 72, 928-935.
45. Serpersu, E. H., Bunk, S., and Schoner, W. (1990) How do magnesium-ATP analogs differentially modify high-affinity and low-affinity ATP binding sites of sodium-potassium ATPase?, Eur. J. Biochem. 191, 397-404.
46. Calvo, C. (1967) The crystal structure of a-magnesium pyrophosphate, Acta Crystallogr. 23, 289-295.
47. Shorter, A. L., Haromy, T. P., Scalzo-Brush, T., Knight, W. B., Dunaway-Mariano, D., and Sundaralingam, M. (1987) Structural and biochemical properties of bidentate tetraaquarhodium(III) complexes of inorganic pyrophosphate and adenosine 5′-diphosphate, Biochemistry 26, 2060-2066.
48. Sanders, C. R., II, Tian, G., and Tsai, M. D. (1989) Mechanism of adenylate kinase. Is there a relationship between local substrate dynamics, and local binding energy, and the catalytic mechanism?, Biochemistry 28, 9028-9043.
49. Torres, L. M., and Marzilli, L. G. (1991) Selective recognition and coordination by the [RhIII(tris(aminoethyl)amine)(H2O)2]3+ cation of the adenine nucleobase only when it is a constituent of a 5′-nucleotide, J. Am. Chem. Soc. 113, 4678-4679.
50. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity, Annu. Rev. Biochem. 62, 685-713.