Probing the interaction of archaeal DNA polymerases with deaminated bases using X-ray crystallography and non-hydrogen bonding isosteric base analogues

Biochemistry

Volumn 49, Issue 27, 2010, Pages 5772-5781

  Killelea, Tom ^a   Ghosh, Samantak ^b   Tan, Samuel S ^b   Heslop, Pauline ^a   Firbank, Susan J ^a   Kool, Eric T ^b   Connolly, Bernard A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ARCHAEAL; DEAMINATED BASIS; DIFLUOROBENZENE; DNA POLYMERASE; DOUBLE STRANDED DNA; EXONUCLEASE; HYDROGEN BONDINGS; ISOSTERIC; N-TERMINAL DOMAINS; NON-POLAR; POLAR PROTEINS; PRIMER STRAND; PROTEIN-DNA INTERACTIONS; RELATIVE IMPORTANCE; RESIDUAL INTERACTIONS; SHAPE RECOGNITION; SINGLE-STRANDED REGION; SPECIFIC RECOGNITION; TEMPLATE JUNCTION; URACIL BINDINGS; X RAY CRYSTAL STRUCTURES;

CRYSTAL STRUCTURE; DNA; HYDROGEN; MOLECULAR VIBRATIONS; POLYMERS; X RAY CRYSTALLOGRAPHY;

HYDROGEN BONDS;

DNA BASE; DNA POLYMERASE; DOUBLE STRANDED DNA; EXONUCLEASE; HYPOXANTHINE; URACIL; ARCHAEAL DNA; DNA; DNA DIRECTED DNA POLYMERASE; INORGANIC COMPOUND; PRIMER DNA; SINGLE STRANDED DNA;

ARCHAEBACTERIUM; ARTICLE; CRYSTAL STRUCTURE; DNA HAIRPIN; DNA TEMPLATE; ENZYME ACTIVE SITE; HYDROGEN BOND; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; STRUCTURE ANALYSIS; THERMOCOCCUS; THERMOCOCCUS GORGONARIUS; X RAY CRYSTALLOGRAPHY; BINDING SITE; CHEMISTRY; DEAMINATION; DNA REPLICATION; GENETICS; METABOLISM; X RAY;

ARCHAEA; THERMOCOCCUS GORGONARIUS;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DEAMINATION; DNA; DNA PRIMERS; DNA REPLICATION; DNA, ARCHAEAL; DNA, SINGLE-STRANDED; DNA-DIRECTED DNA POLYMERASE; EXONUCLEASES; HYDROGEN BONDING; HYPOXANTHINE; INORGANIC CHEMICALS; URACIL; X-RAYS;

EID: 77954697901     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100421r     Document Type: Article

References (44)

1. Greagg, M. A., Fogg, M. J., Panayotou, G., Evans, S. J., Connolly, B. A., and Pearl, L. H. (1999)Aread-ahead function in archaealDNA polymerases detects promutagenic template-strand uracil. Proc. Natl. Acad. Sci. U.S.A. 96, 9045-9050.
2. Fogg, M. J., Pearl, L. H., and Connolly, B. A. (2002) Structural basis for uracil recognition by archaeal family B DNA polymerases. Nat. Struct. Biol. 9, 922-927.
3. Shuttleworth, G., Fogg, M. J., Kurpiewski, M. R., Jen-Jacobson, L., and Connolly, B. A. (2004) Recognition of the Pro-mutagenic Base Uracil by Family B DNA Polymerases from Archaea. J. Mol. Biol. 337, 621-634.
4. Firbank, S. J., Wardle, J., Heslop, P., Lewis, R. J., and Connolly, B. A. (2008) Uracil Recognition in Archaeal DNA Polymerases Captured by X-ray Crystallography. J. Mol. Biol. 381, 529-539.
5. Gill, S., O'Neill, R., Lewis, R. J., and Connolly, B. A. (2007) Interaction of the family-B DNA polymerase from the archaeon Pyrococcus furiosus with deaminated bases. J. Mol. Biol. 372, 855-863.
6. Russell, H. J., Richardson, T. T., Emptage, K., and Connolly, B. A. (2009) The 30-50 proofreading exonuclease of archaeal family-B DNA polymerase hinders the copying of template strand deaminated bases. Nucleic Acids Res. 37, 7603-7611.
7. Wardle, J., Burgers, P. M. J., Cann, I. K. O., Darley, K., Heslop, P., Johansson, E., Lin, L.-J., McGlynn, P., Sanvoisin, J., Stith, C. M., and Connolly, B. A. (2008) Uracil recognition by replicative DNA polymerases is limited to the archaea, not occurring with bacteria and eukarya. Nucleic Acids Res. 36, 793-802.
8. Emptage, K., O'Neill, R., Solovyova, A., and Connolly, B. A. (2008) Interplay between DNA polymerase and proliferating cell nuclear antigen switches off base excision repair of uracil and hypoxanthine during replication in archaea. J. Mol. Biol. 383, 762-771.
9. Schweitzer, B. A., and Kool, E. T. (1994) Nonpolar aromatic nucleosides as hydrophobic isosteres of DNA nucleosides. J. Org. Chem. 59, 7238-7242.
10. Kool, E. T. (2002) Replacing the nucleobases in DNA with designer molecules. Acc. Chem. Res. 35, 936-943.
11. Krueger, A. T., and Kool, E. T. (2007) Model systems for understanding DNA base pairing. Curr. Opin. Chem. Biol. 11, 588-594.
12. Kim, T. W., Delaney, J. C., Essigmann, J. M., and Kool, E. T. (2005) Probing the Active Site Tightness of DNA Polymerase in Sub- Angstrom Increments. Proc. Natl. Acad. Sci. U.S.A. 102, 15803-15808.
13. Kool, E. T., Morales, J. C., and Guckian, K. M. (2000) Mimicking the structure and function of DNA: Insights into DNA stability and replication. Angew. Chem., Int. Ed. 39, 990-1009.
14. Kool, E. T. (2001) Hydrogen bonding, base stacking, and steric effects in DNA replication. Annu. Rev. Biophys. Biomol. Struct. 30, 1-22.
15. Kool, E. T., and Sintim, H. O. (2006) The difluorotoluene debate: A decade later. Chem. Commun., 3665-3675.
16. Potapova, O., Chan, C., DeLucia, A. M., Helquist, S. A., Kool, E. T., Grindley, N. D. F., and Joyce, C. M. (2006) DNA polymerase catalysis in the absence of Watson-Crick hydrogen Bonds: Analysis by single-turnover kinetics. Biochemistry 45, 890-898.
17. Wolfle, W. T., Washington, M. T., Kool, E. T., Spratt, T. E., Helquist, S. A., Prakash, L., and Prakash, S. (2005) Evidence for a Watson- Crick hydrogen bonding requirement in DNA synthesis by human DNA polymerase κ. Mol. Cell. Biol. 25, 7137-7143.
18. Irimia, A., Eoff, R. L., Pallan, P. S., Guengerich, F. P., and Egli, M. (2007) Structure and activity of Y-classDNApolymerase DPO4 from Sulfolobus solfataricus with templates containing the hydrophobic thymine analog 2,4-difluorotoluene. J. Biol. Chem. 282, 36421-36433.
19. Morales, J. C., and Kool, E. T. (2000) Importance of Terminal Base Pair Hydrogen-Bonding in 30-End Proofreading by the Klenow Fragment of DNA Polymerase I. Biochemistry 39, 2626-2632.
20. Francis, A. W., Helquist, S. A., Kool, E. T., and David, S. S. (2003) Probing the Requirements for Recognition and Catalysis in Fpg and MutY with Nonpolar Adenine Isosteres. J. Am. Chem. Soc. 125, 16235-16242.
21. Evans, S. J., Fogg, M. J., Mamone, A., Davis, M., Pearl, L. H., and Connolly, B. A. (2000) Improving dideoxynucleotide-triphosphate utilization by the hyper-thermophilic DNA polymerase from Pyrococcus furiosus. Nucleic Acids Res. 28, 1059-1066.
22. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography, Vol.26.
23. Evans, P. R. (1993) Data reduction. Proceedings of the CCP4 Study Weekend on Data Collection and Processing, 114-122.
24. Collaborative Computational Project Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr. D50, 760-763.
25. Vagin,A., andTeplyakov,A. (1997)MOLREP: Anautomatedprogram for molecular replacement. J. Appl. Crystallogr. 30, 1022-1025.
26. Emsley, P., and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132.
27. Murshudov, G., Vagin, A., and Dodson, E. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255.
28. Kleywegt, G. J. (1996) Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D52, 842-857.
29. Lai, J. S., Qu, J., and Kool, E. T. (2003) Fluorinated DNA bases as probes of electrostatic effects in DNA base stacking. Angew. Chem., Int. Ed. 42, 5973-5977.
30. Seela, F., Bourgeois, W., Rosemeyer, H., and Wenzel, T. (1996) Helv. Chim. Acta 79, 488-498.
31. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complex of a Pol α familyDNApolymerase. Cell 105, 657-666.
32. Shamoo, Y., and Steitz, T. A. (1999) Building a replisome from interacting pieces: Sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell 99, 155-166.
33. Hopfner, K.-P., Eichinger, A., Engh, R. A., Laue, F., Ankenbauer, W., Huber, R., and Angerer, B. (1999) Crystal structure of a thermostable type BDNApolymerase from Thermococcus gorgonarius. Proc. Natl. Acad. Sci. U.S.A. 96, 3600-3605.
34. Beese, L. S., and Steitz, T. A. (1991) Structural basis for the 30-50 exonuclease activity of Escherichia coli DNA polymerase I: A two metal ion mechanism. EMBO J. 10, 25-33.
35. Kim, S. H., Kim, D.-U., Kim, J. K., Kang, L. W., and Cho, H.-S. (2008) Crystal structure of Pfu, the high fidelity polymerase from Pyrococcus furiosus. Int. J. Biol. Macromol. 42, 356-361.
36. Carver, T. E., Jr., Sexton, D. J., and Benkovic, S. J. (1997) Dissociation of bacteriophage T4 DNA polymerase and its processivity clamp after completion of Okazaki fragment synthesis. Biochemistry 36, 14409-14417.
37. Pearl, L. H. (2000) Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res. 460, 165-181.
38. Huffman, J. L., Sundheim, O., and Tainer, J. A. (2006) Structural features of DNA glycosylases and AP endonucleases. In DNA damage recognition (Siede, W., Kow, Y. W., and Doetsch, P. W., Eds.) pp 299-321, Taylor and Francis, New York.
39. Hogg, M., Aller, P., Konigsberg, W., Wallace, S. S., and Doublié, S. (2007) Structural and biochemical investigation of the role in proofreading of a β hairpin loop found in the exonuclease domain of a replicative DNA polymerase of the B family. J. Biol. Chem. 282, 1432-1444.
40. Trzenecka, A., Pzochocka, D., and Bebenek, A. (2009) Different behaviors in vivo of mutations in the β hairpin loop of the DNA polymerases of the closely related phages T4 and RB69. J. Mol. Biol. 289, 797-807.
41. Hashimoto, H., Nishioka, M., Fujiwara, S., Takagi, M., Imanaka, T., Inoue, T., and Kai, Y. (2001) Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. J. Mol. Biol. 306, 469-477.
42. Liu, S., Knafels, J. D., Chang, J. S., Waszak, G. A., Baldwin, E. T., Deibel, M. R., Thomsen, D. R., Homa, F. L., Wells, P. A., Tory, M. C., Poorman, R. A., Gao, H., Qiu, X., and Seddon, A. P. (2006) Crystal structure of the herpes simplex virus 1 DNA polymerase. J. Biol. Chem. 281, 18193-18200.
43. Vallur, A. C., Feller, J. A., Abner, C. W., Tran, R. K., and Bloom, L. B. (2002) Effects of hydrogen bonding within a damaged base pair on the activity of wild type and DNA-intercalating mutants of human alkyladenine DNA glycosylase. J. Biol. Chem. 277, 31673-31678.
44. Chepanoske, C. L., Langlier, C. R., Chmiel, N. H., and David, S. S. (2000) Recognition of the nonpolar base 4-methylindole in DNA by the DNA repair adenine glycosylase MutY. Org. Lett. 2, 1341-1344.