Dimerization of the Klenow fragment of Escherichia coli DNA polymerase I is linked to its mode of DNA binding

Biochemistry

Volumn 46, Issue 27, 2007, Pages 8085-8099

  Bailey, Michael F ^a,b   Van Der Schans, Edwin J C ^a   Millar, David P ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOPHYSICAL TECHNIQUES; ESCHERICHIA COLI DNA POLYMERASE; PROOFREADING POLYMERASE;

COMPLEXATION; DNA; ELECTROPHORESIS; ESCHERICHIA COLI; POLYMERIZATION; STOICHIOMETRY;

ENZYME KINETICS;

DNA DIRECTED DNA POLYMERASE BETA; OLIGODEOXYRIBONUCLEOTIDE; PRIMER DNA;

ANALYTIC METHOD; ANISOTROPY; ARTICLE; COMPLEX FORMATION; DIMERIZATION; DNA BINDING; DNA REPLICATION; DNA TEMPLATE; ELECTROPHORETIC MOBILITY; ENZYME ACTIVE SITE; ESCHERICHIA COLI; FLUORESCENCE; MEASUREMENT; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; STOICHIOMETRY; TITRIMETRY; ULTRACENTRIFUGATION;

BASE SEQUENCE; BINDING SITES; DIMERIZATION; DNA POLYMERASE I; DNA PRIMERS; DNA, BACTERIAL; DNA-DIRECTED DNA POLYMERASE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; FLUORESCENCE POLARIZATION; TEMPLATES, GENETIC;

ESCHERICHIA COLI;

EID: 34447345149     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi6024148     Document Type: Article

References (42)

1. Brutlag, D., Atkinson, M. R., Setlow, P., and Kornberg, A. (1969) An active fragment of DNA polymerase produced by proteolytic cleavage, Biochem. Biophys. Res. Commun. 37, 982-989.
2. 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.
3. Wang, J., Sattar, A. K. M. A., Wang, C. C., Karam, J. D., Konigsberg, W. H., and Steitz, T. A. (1997) Crystal structure of a pol α family replication DNA polymerase from bacteriophage RB69, Cell 89, 1087-1099.
4. 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 264, 1930-1935.
5. Trincao, J., Johnson, R. E., Escalante, C. R., Prakash, S., Prakash, L., and Aggarwal, A. K. (2001) Structure of the catalytic core of S. cerevisiae DNA polymerase η: Implications for translesion DNA synthesis, Mol. Cell 8, 417-426.
6. Zhou, B.-L., Pata, J. D., and Steitz, T. A. (2001) Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain, Mol. Cell 8, 427-437.
7. 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.
8. 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.
9. 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.
10. Washington, M. T., Prakash, L., and Prakash, S. (2001) Yeast DNA polymerase η utilizes an induced-fit mechanism for nucleotide incorporation, Cell 107, 917-927.
11. Fiala, K. A., and Suo, Z. (2004) Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV, Biochemistry 43, 2116-2125.
12. Derbyshire, V., Freemont, P. S., Sanderson, M. R., Beese, L., Friedman, J. M., Joyce, C. M., and Steitz, T. A. (1998) Genetic and crystallographic studies of the 3′,5′-exonucleolytic site of DNA polymerase I, Science 240, 199-201.
13. Beese, L. S., Friedman, J., and Steitz, T. A. (1993) Crystal structures of the Klenow fragment of DNA polymerase I complexed with deoxynucleoside triphosphate and pyrophosphate, Biochemistry 32, 14095-14101.
14. Cowart, M., Gibson, K. J., Allen, D. J., and Benkovic, S. J. (1989) DNA substrate requirements for exonuclease and polymerase activities of prokaryotic and phage DNA polymerases, Biochemistry 28, 1975-1983.
15. Ruscitti, T., Polayes, D. A., Kara, A. E., and Linn, S. (1992) Selective immunoneutralization of the multiple activities of Escherichia coli DNA polymerase I supports the model for separate active sites and indicates a complex 5′ to 3′ exonuclease, J. Biol. Chem. 267, 16806-16811.
16. Freemont, P. S., Friedman, J. M., Beese, L. S., Sanderson, M. R., and Steitz, T. A. (1998) Cocrystal structure of an editing complex of Klenow fragment with DNA, Proc. Natl. Acad. Sci. U.S.A. 85, 8924-8928.
17. Li, Y., Korolev, S., and Waksman, G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: Structural basis for nucleotide incorporation, EMBO J. 17, 7514-7525.
18. Doublie, S., Tabor, S., Long, A. M., Richardson, C. C., and Ellenberger, T. (1998) Crystal structure of bacteriophage T7 replication complex at 2.2 A resolution, Nature 391, 251-258.
19. Beese, L. S., Derbyshire, V., and Steitz, T. A. (1993) Structure of DNA polymerase I Klenow fragment bound to duplex DNA, Science 260, 352-355.
20. Carver, T. E., Hochstrasser, R. A., and Millar, D. P. (1994) Proofreading DNA: Recognition of aberrant DNA termini by the Klenow fragment of DNA polymerase I, Proc. Natl. Acad. Sci. U.S.A. 91, 10670-10674.
21. Bailey, M. F., Thompson, E. H. Z., and Millar, D. P. (2001) Probing DNA polymerase fidelity mechanisms using time-resolved fluorescence anisotropy, Methods 25, 62-77.
22. Eis, P. E., and Millar, D. P. (1993) Conformational distributions of a four-way DNA junction revealed by time-resolved fluorescence resonance energy transfer, Biochemistry 32, 13852-13860.
23. Warshaw, M. M., and Cantor, C. R. (1970) Oligonucleotide interactions. IV. Conformational differences between deoxy- and ribodinucleoside phosphates, Biopolymers 9, 1079-1103.
24. Joyce, C. M., and Derbyshire, V. (1995) Purification of E. coli DNA polymerase 1 and Klenow fragment, Methods Enzymol. 262, 3-13.
25. Schuck, P. (1998) Sedimentation analysis of noninteracting and self-associating solutes using numerical solutions to the Lamm equation, Biophys. J. 75, 1503-1512.
26. Allen, D. J., Darke, P. L., and Benkovic, S. J. (1989) Fluorescent oligonucleotides and deoxynucletide triphosphates: Preparation and their interaction with the large (Klenow) fragment of Escherichia coli DNA polymerase I, Biochemistry 28, 4601-4607.
27. Laue, T. M., Senear, D. F., Eaton, S., and Ross, J. B. A. (1993) 5-Hydroxytryptophan as a new intrinsic probe for investigating protein-DNA interactions by analytical ultracentrifugation. Study of the effect of DNA on the self-assembly of the λ cI repressor, Biochemistry 32, 2469-2472.
28. Schuk, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation, Anal. Biochem. 320, 104-124.
29. Howlett, G. J., Minton, A. P., and Rivas, G. (2006) Analytical ultracentrifugation studies of protein associations and assembly, Curr. Opin. Chem. Biol. 10, 430-436.
30. Bailey, M. F., Van der Schans, E. J. C., and Millar, D. P. (2004) Thermodynamic dissection of the polymerizing and editing modes of a DNA polymerase, J. Mol. Biol. 336, 673-693.
31. Guest, C. R., Hochstrasser, R. A., Dupuy, C. G., Allen, D. J., Benkovic, S. J. and Millar, D. P. (1991) Interaction of DNA with DNA polymerase I studied by time-resolved fluorescence spectroscopy, Biochemistry 30, 8759-8770.
32. Derbyshire, V., Grindley, N. D. F., and Joyce, C. M. (1991) The 3′-5′ exonuclease of DNA polymerase I of Eschericia coli: Contribution of each amino acid at the active site to the reaction, EMBO J. 10, 17-24.
33. Catalano, C. E., Allen, D. J., and Benkovic, S. J. (1990) Interaction of Escherichia coli DNA polymerase I with azidoDNA and dfluorescent DNA probes: Identification of protein-DNA contacts, Biochemistry 29, 3612-3621.
34. Hochstrasser, R. A., Carver, T. E., Sowers, L. C., and Millar, D. P. (1994) Melting of a DNA helix terminus within the active site of a DNA polymerase, Biochemistry 33, 11971-11979.
35. 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.
36. Astatke, M., Grindley, N. D. F., and Joyce, C. M. (1995) Deoxynucleoside triphophate 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.
37. Rechkoblit, O., Amin, S., and Geacintov, N. E. (1999) Primer length dependence of binding of DNA polymerase I Klenow fragment to template-primer complexes containing site-specific bulky lesions, Biochemistry 38, 11834-11843.
38. Munn, M. M., and Alberts, B. M. (1991) DNA footprinting studies of the complex formed by the T4 DNA polymerase holoenzyme at a primer-template junction, J. Biol. Chem. 266, 20034-20044.
39. Debsyer, Z., Tabor, S., and Richardson, C. C. (1994) Coordination of leading and lagging strand synthesis at the replication fork of bacteriophage T7, Cell 77, 157-166.
40. Lee, J., Chastain, P. D., Kusakabe, T., Griffith, J., and Richardson, C. C. (1998) Coordinated leading and lagging strand synthesis on a minicircular template, Mol. Cell 1, 1001-1010.
41. Kim, S., Dallmann, H. G., McHenry, C. S., and Marians, K. J. (1996) T couples the leading- and lagging-strand polymerases at the Escherichia coli replication fork, J. Biol. Chem. 271, 21406-21412.
42. Marians, K. J., Hiasa, H., Kim, D. R., and McHenry, C. S. (1998) Role of the core DNA polymerase III subunits at the replication fork, a is the only subunit required for processive replication, J. Biol. Chem. 273, 2452-2457.