Use of 2-aminopurine fluorescence to examine conformational changes during nucleotide incorporation by DNA polymerase I (Klenow fragment)

Biochemistry

Volumn 42, Issue 34, 2003, Pages 10200-10211

  Purohit, Vandana ^a   Grindley, Nigel D F ^a   Joyce, Catherine M ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDES;

DNA; ENZYMES; FLUORESCENCE;

CONFORMATIONS;

2 AMINOPURINE; DEOXYNUCLEOSIDE TRIPHOSPHATE; DNA; DNA DIRECTED DNA POLYMERASE BETA; NUCLEOSIDE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DNA BINDING; DNA CONFORMATION; DNA STRUCTURE; DNA TEMPLATE; ENZYME SUBSTRATE; FLUORESCENCE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

2-AMINOPURINE; BASE SEQUENCE; BINDING SITES; DEOXYRIBONUCLEOTIDES; DNA POLYMERASE I; DNA PRIMERS; FLUORESCENT DYES; KINETICS; MAGNESIUM; MANGANESE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; SUBSTRATE SPECIFICITY; TEMPLATES, GENETIC; THYMINE NUCLEOTIDES;

EID: 0041823551     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0341206     Document Type: Article

References (54)

1. Ollis, D. L., Brick, P., Hamlin, R., Xuong, N. G., and Steitz, T. A. (1985) Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP, Nature 313, 762-766.
2. Steitz, T. A. (1999) DNA polymerases: structural diversity and common mechanisms, J. Biol. Chem. 274, 17395-17398.
3. Benkovic, S. J., and Cameron, C. E. (1995) Kinetic analysis of nucleotide incorporation and misincorporation by Klenow fragment of Escherichia coli DNA polymerase I, Methods Enzymol. 262, 257-269.
4. Joyce, C. M., and Steitz, T. A. (1994) Function and structure relationships in DNA polymerases, Annu. Rev. Biochem. 63, 777-822.
5. Brautigam, C. A., and Steitz, T. A. (1998) Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes, Curr. Opin. Struct. Biol. 8, 54-63.
6. Li, Y., Korolev, S., and Waksman, G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation, EMBO J. 17, 7514-7525.
7. Kiefer, J. R., Mao, C., Braman, J. C., and Beese, L. S. (1998) Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal, Nature 391, 304-307.
8. Johnson, S. J., Taylor, J. S., and Beese, L. S. (2003) Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations, Proc. Natl. Acad. Sci. U.S.A. 100, 3985-3900.
9. Doublié, S., Tabor, S., Long, A., Richardson, C. C., and Ellenberger, T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution, Nature 391, 251-258.
10. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complex of a pol α family DNA polymerase, Cell 105, 657-667.
11. Huang, H., Chopra, R., Verdine, G. L., and Harrison, S. C. (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance, Science 282, 1669-1675.
12. 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.
13. Holm, L., and Sander, C. (1995) DNA polymerase β belongs to an ancient nucleotidyltransferase superfamily, Trends Biochem. Sci. 20, 345-347.
14. 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.
15. 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, 4835-4843.
16. Eger, B. T., and Benkovic, S. J. (1992) Minimal kinetic mechanism for misincorporation by DNA polymerase I (Klenow fragment), Biochemistry 31, 9227-9236.
17. Carroll, S. S., Cowart, M., and Benkovic, S. J. (1991) A mutant of DNA polymerase I (Klenow fragment) with reduced fidelity, Biochemistry 30, 804-813.
18. Minnick, D. T., Liu, L., Grindley, N. D. F., Kunkel, T. A., and Joyce, C. M. (2002) Discrimination against purine-pyrimidine mispairs in the polymerase active site of DNA polymerase I: a structural explanation, Proc. Natl. Acad. Sci. U.S.A. 99, 1194-1199.
19. Wong, I., Patel, S. S., and Johnson, K. A. (1991) An induced-fit kinetic mechanism for DNA replication fidelity: direct measurement by single-turnover kinetics, Biochemistry 30, 526-537.
20. 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, 8410-8417.
21. Herschlag, D., Piccirilli, J. A., and Cech, T. R. (1991) Ribozyme-catalyzed and nonenzymatic reactions of phosphate diesters: rate effects upon substitution of sulfur for a nonbridging phosphoryl oxygen atom, Biochemistry 30, 4844-4854.
22. Polesky, A. H., Dahlberg, M. E., Benkovic, S. J., Grindley, N. D. F., and Joyce, C. M. (1992) Side chains involved in catalysis of the polymerase reaction of DNA polymerase I from Escherichia coli, J. Biol. Chem. 267, 8417-8428.
23. Capson, T. L., Peliska, J. A., Kaboord, B. F., Frey, M. W., Lively, C., Dahlberg, M., and Benkovic, S. J. (1992) Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4, Biochemistry 31, 10984-10994.
24. Showalter, A. K., and Tsai, M.-D. (2002) A reexamination of the nucleotide incorporation fidelity of DNA polymerases, Biochemistry 41, 10571-10576.
25. Doublié, S., Sawaya, M. R., and Ellenberger, T. (1999) An open and closed case for all polymerases, Struct. Folding Des. 7, R31-35.
26. Shah, A. M., Li, S.-X., Anderson, K. S., and Sweasy, J. B. (2001) Y265H mutator mutant of DNA polymerase β. Proper geometric alignment is critical for fidelity, J. Biol. Chem. 276, 10824-10831.
27. 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.
28. Zhong, X., Patel, S. S., and Tsai, M.-D. (1998) DNA polymerase β. Dissecting the functional roles of the two metal ions with Cr-(III)dTTP, J. Am. Chem. Soc. 120, 235-236.
29. 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.
30. Sowers, L. C., Fazakerley, G. V., Eritja, R., Kaplan, B. E., and Goodman, M. F. (1986) Base pairing and mutagenesis: observation of a protonated base pair between 2-aminopurine and cytosine in an oligonucleotide by proton NMR, Proc. Natl. Acad. Sci. U.S.A. 83, 5434-5438.
31. Rachofsky, E. L., Osman, R., and Ross, J. B. A. (2001) Probing structure and dynamics of DNA with 2-aminopurine: effects of local environment on fluorescence, Biochemistry 40, 946-956.
32. 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.
33. Jia, Y., Kumar, A., and Patel, S. S. (1996) Equilibrium and stopped-flow kinetic studies of interaction between T7 RNA polymerase and its promoters measured by protein and 2-aminopurine fluorescence changes, J. Biol. Chem. 271, 30451-30458.
34. Mandal, S. S., Fidalgo da Silva, E., and Reha-Krantz, L. J. (2002) Using 2-aminopurine fluorescence to detect base unstacking in the template strand during nucleotide incorporation by the bacteriophage T4 DNA polymerase, Biochemistry 41, 4399-4406.
35. 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.
36. Derbyshire, V., Freemont, P. S., Sanderson, M. R., Beese, L., Friedman, J. M., Joyce, C. M., and Steitz, T. A. (1988) Genetic and crystallographic studies of the 3′,5′-exonucleolytic site of DNA polymerase I, Science 240, 199-201.
37. Joyce, C. M., and Derbyshire, V. (1995) Purification of E. coli DNA polymerase I and Klenow fragment, Methods Enzymol. 262, 3-13.
38. Turner, R. M., Jr., Grindley, N. D. F., and Joyce, C. M. (2003) Interaction of DNA polymerase I (Klenow fragment) with the single stranded template beyond the site of synthesis, Biochemistry 42, 2373-2385.
39. Astatke, M., Grindley, N. D. F., and Joyce, C. M. (1998) How E. coli DNA polymerase I (Klenow fragment) distinguishes between deoxy- and dideoxynucleotides, J. Mol. Biol. 278, 147-165.
40. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
41. Smith, R. M., Martell, A. E., and Chen, Y. (1991) Critical Evaluation of Stability Constants for Nucleotide Complexes with Protons and Metal Ions, Pure Appl. Chem. 63, 1015-1080.
42. Bloom, L. B., Otto, M. R., Beechem, J. M., and Goodman, M. F. (1993) Influence of 5′-nearest neighbors on the insertion kinetics of the fluorescent nucleotide analogue 2-aminopurine by Klenow fragment, Biochemistry 32, 11247-11258.
43. Li, Y., and Waksman, G. (2001) Crystal structures of a ddATP-, ddTTP-, ddCTP-, and ddGTP-trapped ternary complex of Klentaq1: insights into nucleotide incorporation and selectivity, Protein Sci. 10, 1225-1233.
44. Li, Y., Kong, Y., Korolev, S., and Waksman, G. (1998) Crystal structures of the Klenow fragment of Thermus aquaticus DNA polymerase I complexed with deoxyribonucleoside triphosphates, Protein Sci. 7, 1116-1123.
45. Fidalgo da Silva, E., Mandal, S. S., and Reha-Krantz, L. J. (2002) Using 2-aminopurine fluorescence to measure incorporation of incorrect nucleotides by wild type and mutant bacteriophage T4 DNA polymerases, J. Biol. Chem. 277, 40640-40649.
46. Dzantiev, L., Alekseyev, Y. O., Morales, J. C., Kool, E. T., and Romano, L. J. (2001) Significance of nucleobase shape complementarity and hydrogen bonding in the formation and stability of the closed polymerase-DNA complex, Biochemistry 40, 3215-3221.
47. Dzantiev, L., and Romano, L. J. (2000) A conformational change in E. coli DNA polymerase I (Klenow fragment) is induced in the presence of a dNTP complementary to the template base in the active site, Biochemistry 39, 356-361.
48. Astatke, M., Grindley, N. D. F., and Joyce, C. M. (1995) Deoxynucleoside triphosphate and pyrophosphate binding sites in the catalytically competent ternary complex for the polymerase reaction catalyzed by DNA polymerase I (Klenow fragment), J. Biol. Chem. 270, 1945-1954.
49. Yang, G., Franklin, M., Li, J., Lin, T. C., and Konigsberg, W. (2002) Correlation of the kinetics of finger domain mutants in RB69 DNA polymerase with its structure, Biochemistry 41, 2526-2534.
50. 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.
51. 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.
52. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity, Annu. Rev. Biochem. 62, 685-713.
53. Post, C. B., and Ray, W. J., Jr. (1995) Reexamination of induced fit as a determinant of substrate specificity in enzymatic reactions, Biochemistry 34, 15881-15885.
54. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb Viewer: an environment for comparative protein modeling, Electrophoresis 18, 2714-2723.