Conformational landscapes of DNA polymerase i and mutator derivatives establish fidelity checkpoints for nucleotide insertion

Nature Communications

Volumn 4, Issue , 2013, Pages

  Hohlbein, Johannes ^a,c   Aigrain, Louise ^a   Craggs, Timothy D ^a,b   Bermek, Oya ^b,d   Potapova, Olga ^b   Shoolizadeh, Pouya ^a   Grindley, Nigel D F ^b   Joyce, Catherine M ^b   Kapanidis, Achillefs N ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b YALE UNIVERSITY   (United States)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; MUTANT PROTEIN; NUCLEOTIDE;

BIOCHEMISTRY; DNA; MUTATION; PHENOTYPE;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; DNA SYNTHESIS; ENERGY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PHENOTYPE; STEADY STATE;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; DNA POLYMERASE I; DNA REPLICATION; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; GEOBACILLUS STEAROTHERMOPHILUS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, INSERTIONAL; NUCLEOTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84880318919     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3131     Document Type: Article

References (32)

1. Kunkel, T. A. & Bebenek, K. DNA replication fidelity. Annu. Rev. Biochem. 69, 497-529 (2000).
2. Joyce, C. M. & Benkovic, S. J. DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry 43, 14317-14324 (2004). (Pubitemid 39491965)
3. Doublié, S., Sawaya, M. R. & Ellenberger, T. An open and closed case for all polymerases. Structure 7, R31-R35 (1999). (Pubitemid 29159696)
4. Johnson, S. J., Taylor, J. S. & Beese, L. S. Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations. Proc. Natl Acad. Sci. USA 100, 3895-3900 (2003). (Pubitemid 36418128)
5. Kool, E. T. Active site tightness and substrate fit in DNA replication. Annu. Rev. Biochem. 71, 191-219 (2002). (Pubitemid 34800219)
6. Li, Y., Korolev, S. & Waksman, G. 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 (1998). (Pubitemid 29002718)
7. Santoso, Y. et al. Conformational transitions in DNA polymerase I revealed by single-molecule FRET. Proc. Natl Acad. Sci. USA 107, 715-720 (2010).
8. Santoso, Y., Torella, J. P. & Kapanidis, A. N. Characterizing single-molecule FRET dynamics with probability distribution analysis. Chem. Phys. Chem. 11, 2209-2219 (2010).
9. Santoso, Y. & Kapanidis, A. N. Probing biomolecular structures and dynamics of single molecules using in-gel alternating-laser excitation. Anal. Chem. 81, 9561-9570 (2009).
10. Torella, J. P., Holden, S. J., Santoso, Y., Hohlbein, J. & Kapanidis, A. N. Identifying molecular dynamics in single-molecule FRET experiments with burst variance analysis. Biophys. J. 100, 1568-1577 (2011).
11. Bell, J. B., Eckert, K. A., Joyce, C. M. & Kunkel, T. A. Base miscoding and strand misalignment errors by mutator Klenow polymerases with amino acid substitutions at tyrosine 766 in the O helix of the fingers subdomain. J. Biol. Chem. 272, 7345-7351 (1997). (Pubitemid 27166444)
12. Minnick, D. T. et al. Side chains that influence fidelity at the polymerase active site of Escherichia coli DNA polymerase I (Klenow fragment). J. Biol. Chem. 274, 3067-3075 (1999). (Pubitemid 29075395)
13. Minnick, D. T., Liu, L., Grindley, N. D. F., Kunkel, T. A. & Joyce, C. M. Discrimination against purine-pyrimidine mispairs in the polymerase active site of DNA polymerase I: a structural explanation. Proc. Natl Acad. Sci. USA 99, 1194-1199 (2002). (Pubitemid 34136469)
14. Carroll, S. S., Cowart, M. & Benkovic, S. J. A mutant of DNA polymerase I (Klenow fragment) with reduced fidelity. Biochemistry 30, 804-813 (1991).
15. Astatke, M., Grindley, N. D. F. & Joyce, C. M. How E. coli DNA polymerase I (Klenow fragment) distinguishes between deoxy-and dideoxynucleotides. J. Mol. Biol. 278, 147-165 (1998). (Pubitemid 28196157)
16. Astatke, M., Ng, K. M., Grindley, N. D. F. & Joyce, C. M. A single side chain prevents Escherichia coli DNA polymerase I (Klenow fragment) from incorporating ribonucleotides. Proc. Natl Acad. Sci. USA 95, 3402-3407 (1998). (Pubitemid 28173140)
17. Kalinin, S., Felekyan, S., Antonik, M. & Seidel, C. A. M. Probability distribution analysis of single-molecule fluorescence anisotropy and resonance energy transfer. J. Phys. Chem. B 111, 10253-10262 (2007). (Pubitemid 47388032)
18. Antonik, M., Felekyan, S., Gaiduk, A. & Seidel, C. A. M. Separating structural heterogeneities from stochastic variations in fluorescence resonance energy transfer distributions via photon distribution analysis. J. Phys. Chem. B 110, 6970-6978 (2006). (Pubitemid 43672169)
19. Nir, E. et al. Shot-noise limited single-molecule FRET histograms: comparison between theory and experiments. J. Phys. Chem. B 110, 22103-22124 (2006). (Pubitemid 44806929)
20. Kalinin, S., Valeri, A., Antonik, M., Felekyan, S. & Seidel, C. A. M. Detection of structural dynamics by FRET: a photon distribution and fluorescence lifetime analysis of systems with multiple states. J. Phys. Chem. B 114, 7983-7995 (2010).
21. Wu, E. Y. & Beese, L. S. The structure of a high fidelity DNA polymerase bound to a mismatched nucleotide reveals an 'ajar' intermediate conformation in the nucleotide selection mechanism. J. Biol. Chem. 286, 19758-19767 (2011).
22. Berezhna, S. Y., Gill, J. P., Lamichhane, R. & Millar, D. P. Single-molecule förster resonance energy transfer reveals an innate fidelity checkpoint in DNA polymerase I. J. Am. Chem. Soc. 134, 11261-11268 (2012).
23. Joyce, C. M. et al. Fingers-closing and other rapid conformational changes in DNA polymerase I (Klenow fragment) and their role in nucleotide selectivity. Biochemistry 47, 6103-6116 (2008). (Pubitemid 351812823)
24. Garalde, D. R. et al. Distinct complexes of DNA polymerase I (Klenow fragment) for base and sugar discrimination during nucleotide substrate selection. J. Biol. Chem. 286, 14480-14492 (2011).
25. Bermek, O., Grindley, N. D. F. & Joyce, C. M. Distinct roles of the active-site Mg2\+ ligands, Asp882 and Asp705, of DNA polymerase I (Klenow fragment) during the prechemistry conformational transitions. J. Biol. Chem. 286, 3755-3766 (2011).
26. Luo, G., Wang,M., Konigsberg, W. H. & Xie, X. S. Single-molecule and ensemble fluorescence assays for a functionally important conformational change in T7 DNA polymerase. Proc. Natl Acad. Sci. USA 104, 12610-12615 (2007). (Pubitemid 47255202)
27. Wheeler, L. J., Rajagopal, I. & Mathews, C. K. Stimulation of mutagenesis by proportional deoxyribonucleoside triphosphate accumulation in Escherichia coli. DNA Repair. (Amst). 4, 1450-1456 (2005). (Pubitemid 41653306)
28. Dahlberg, M. E. & Benkovic, S. J. 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 (1991).
29. Beard, W. A. & Wilson, S. H. Structural insights into the origins of DNA polymerase fidelity. Structure 11, 489-496 (2003). (Pubitemid 36579127)
30. Kapanidis, A. N. et al. Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc. Natl Acad. Sci. USA 101, 8936-8941 (2004). (Pubitemid 38781589)
31. Lee, N. K. et al. Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. Biophys. J. 88, 2939-2953 (2005). (Pubitemid 40976158)
32. Holden, S. J. et al. Defining the limits of single-molecule FRET resolution in TIRF microscopy. Biophys. J. 99, 3102-3111 (2010). Framework Program