The L561A substitution in the nascent base-pair binding pocket of RB69 DNA polymerase reduces base discrimination

Biochemistry

Volumn 45, Issue 7, 2006, Pages 2211-2220

  Zhang, Hong ^a   Rhee, Chanu ^a   Bebenek, Anna ^b   Drake, John W ^c   Wang, Jimin ^a   Konigsberg, William ^a  

^a YALE UNIVERSITY   (United States)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOASSAY; CATALYSIS; DNA; MUTAGENESIS; QUENCHING;

BASE SELECTIVITY; CHEMICAL QUENCH ASSAYS; MUTATION FREQUENCY; RB69 DNA POLYMERASE;

ENZYMES;

DNA POLYMERASE; EXONUCLEASE;

AMINO ACID SUBSTITUTION; ARTICLE; BASE PAIRING; BINDING SITE; ENZYME ANALYSIS; ESCHERICHIA COLI; GENE MUTATION; MUTATION RATE; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; WILD TYPE;

ALANINE; AMINO ACID SUBSTITUTION; BASE PAIR MISMATCH; BINDING SITES; DNA-DIRECTED DNA POLYMERASE; LEUCINE; MODELS, MOLECULAR; VIRAL PROTEINS;

ENTEROBACTERIA PHAGE T4; ESCHERICHIA COLI;

EID: 33144478306     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052099y     Document Type: Article

References (49)

1. Kunkel, T. A. (1992) DNA replication fidelity, J. Biol Chem. 267, 18251-4.
2. Echols, H., and Goodman, M. F. (1991) Fidelity mechanisms in DNA replication, Annu. Rev. Biochem. 60, 477-511.
3. Goodman, M. F., Creighton, S., Bloom, L. B., and Petruska, J. (1993) Biochemical basis of DNA replication fidelity, Crit. Rev. Biochem. Mol. Biol. 28, 83-126.
4. Kunkel, T. A., and Bebenek, K. (2000) DNA replication fidelity, Annu. Rev. Biochem. 69, 497-529.
5. Yin, Y. W., and Steitz, T. A. (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase, Science 298, 1387-95.
6. Goodman, M. F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes, Annu. Rev. Biochem. 71, 17-50.
7. Ellenberger, T., and Silvian, L. F. (2001) The anatomy of infidelity, Nat. Struct. Biol. 8, 827-8.
8. Pham, P., Rangarajan, S., Woodgate, R., and Goodman, M. F. (2001) Roles of DNA polymerases V and II in SOS-induced error-prone and error-free repair in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 98, 8350-4.
9. Sutton, M. D., and Walker, G. C. (2001) Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination, Proc. Natl. Acad. Sci. U.S.A. 98, 8342-9.
10. Woodgate, R. (1999) A plethora of lesion-replicating DNA polymerases, Genes Dev. 13, 2191-5.
11. Shen, X., Sayer, J. M., Kroth, H., Ponten, I., O'Donnell, M., Woodgate, R., Jerina, D. M., and Goodman, M. F. (2002) Efficiency and accuracy of SOS-induced DNA polymerases replicating benzo[a]pyrene-7,8-diol 9,10-epoxide A and G adducts, J. Biol. Chem. 277, 5265-74.
12. Freisinger, E., Grollman, A. P., Miller, H., and Kisker, C. (2004) Lesion (in)tolerance reveals insights into DNA replication fidelity, EMBO J. 23, 1494-505.
13. Friedberg, E. C., Fischhaber, P. L., and Kisker, C. (2001) Error-prone DNA polymerases: novel structures and the benefits of infidelity, Cell 107, 9-12.
14. Hubscher, U., Maga, G., and Spadari, S. (2002) Eukaryotic DNA polymerases, Annu. Rev. Biochem. 71, 133-63.
15. Prakash, S., and Prakash, L. (2002) Translesion DNA synthesis in eukaryotes: a one- or two-polymerase affair, Genes Dev. 16, 1872-83.
16. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication, Cell 107, 91-102.
17. 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, 427-37.
18. Ohmori, H., Friedberg, E. C., Fuchs, R. P., Goodman, M. F., Hanaoka, F., Hinkle, D., Kunkel, T. A., Lawrence, C. W., Livneh, Z., Nohmi, T., Prakash, L., Prakash, S., Todo, T., Walker, G. C., Wang, Z., and Woodgate, R. (2001) The Y-family of DNA polymerases, Mol. Cell 8, 7-8.
19. Kunkel, T. A., Pavlov, Y. I., and Bebenek, K. (2003) Functions of human DNA polymerases eta, kappa and iota suggested by their properties, including fidelity with undamaged DNA templates, DNA Repair 2, 135-49.
20. Friedberg, E. C., Wagner, R., and Radman, M. (2002) Specialized DNA polymerases, cellular survival, and the genesis of mutations, Science 296, 1627-30.
21. Boudsocq, F., Ling, H., Yang, W., and Woodgate, R. (2002) Structure-based interpretation of missense mutations in Y-family DNA polymerases and their implications for polymerase function and lesion bypass, DNA Repair 1, 343-58.
22. Beard, W. A., and Wilson, S. H. (2003) Structural insights into the origins of DNA polymerase fidelity, Structure 11, 489-96.
23. Kunkel, T. A. (2004) DNA replication fidelity, J. Biol. Chem. 279, 16895-8.
24. Beard, W. A., Shock, D. D., and Wilson, S. H. (2004) Influence of DNA structure on DNA polymerase beta active site function: extension of mutagenic DNA intermediates, J. Biol. Chem. 279, 31921-9.
25. Braithwaite, D. K., and Ito, J. (1993) Compilation, alignment, and phylogenetic relationships of DNA polymerases, Nucleic Acids Res. 21, 787-802.
26. Wang, J., Sattar, A. K., Wang, C. C., Karam, J. D., Konigsberg, W. H., and Steitz, T. A. (1997) Crystal structure of a pol alpha family replication DNA polymerase from bacteriophage RB69, Cell 89, 1087-99.
27. 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, 155-66.
28. Hogg, M., Wallace, S. S., and Doublie, S. (2004) Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site, EMBO J. 23, 1483-93.
29. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complex of a pol alpha family DNA polymerase, Cell 105, 657-67.
30. Joyce, C. M., and Steitz, T. A. (1994) Function and structure relationships in DNA polymerases, Annu. Rev. Biochem. 63, 777-822.
31. Yang, G., Franklin, M., Li, J., Lin, T. C., and Konigsberg, W. (2002) A conserved Tyr residue is required for sugar selectivity in a Pol a DNA polymerase, Biochemistry 41, 10256-61.
32. 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, 2526-34.
33. Bebenek, A., Dressman, H. K., Carver, G. T., Ng, S., Petrov, V., Yang, G., Konigsberg, W. H., Karam, J. D., and Drake, J. W. (2001) Interacting fidelity defects in the replicative DNA polymerase of bacteriophage RB69, J. Biol. Chem. 276, 10387-97.
34. Yang, G., Wang, J., and Konigsberg, W. (2005) Base selectivity is impaired by mutants that perturb hydrogen bonding networks in the RB69 DNA polymerase active site, Biochemistry 44, 3338-46.
35. Minnick, D. T., Bebenek, K., Osheroff, W. P., Turner, R. M., Jr., Astatke, M., Liu, L., Kunkel, T. A., and Joyce, C. M. (1999) Side chains that influence fidelity at the polymerase active site of Escherichia coli DNA polymerase I (Klenow fragment), J. Biol. Chem. 274, 3067-75.
36. Minnick, D. T., Liu, L., Grindley, N. D., 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, 1194-9.
37. Wang, C. X., Zakharova, E., Li, J., Joyce, C. M., Wang, J., and Konigsberg, W. (2004) Pre-steady-state kinetics of RB69 DNA polymerase and its exo domain mutants: effect of pH and thiophosphoryl linkages on 3′-5′ exonuclease activity, Biochemistry 43, 3853-61.
38. Dressman, H. K., Wang, C. C., Karam, J. D., and Drake, J. W. (1997) Retention of replication fidelity by a DNA polymerase functioning in a distantly related environment, Proc. Natl. Acad. Sci. U.S.A. 94, 8042-6.
39. Petrov, V. M., and Karam, J. D. (2002) RNA determinants of translational operator recognition by the DNA polymerases of bacteriophages T4 and RB69, Nucleic Acids Res. 30, 3341-8.
40. Wang, C. C., Yeh, L. S., and Karam, J. D. (1995) Modular organization of T4 DNA polymerase. Evidence from phylogenetics, J. Biol. Chem. 270, 26558-64.
41. Beard, W. A., Shock, D. D., Vande Berg, B. J., and Wilson, S. H. (2002) Efficiency of correct nucleotide insertion governs DNA polymerase fidelity, J. Biol. Chem. 277, 47393-8.
42. Kennard, O. (1986) Base-pair mismatches in DNA fragments, Biochem. Soc. Trans. 14, 207-10.
43. Bebenek, A., Carver, G. T., Dressman, H. K., Kadyrov, F. A., Haseman, J. K., Petrov, V., Konigsberg, W. H., Karam, J. D., and Drake, J. W. (2002) Dissecting the fidelity of bacteriophage RB69 DNA polymerase: site-specific modulation of fidelity by polymerase accessory proteins, Genetics 162, 1003-18.
44. Johnson, S. J., and Beese, L. S. (2004) Structures of mismatch replication errors observed in a DNA polymerase, Cell 116, 803-16.
45. Skelly, J. V., Edwards, K. J., Jenkins, T. C., and Neidle, S. (1993) Crystal structure of an oligonucleotide duplex containing G·G base pairs: influence of mispairing on DNA backbone conformation, Proc. Natl. Acad. Sci. U.S.A. 90, 804-8.
46. + base pairs, Biochemistry 37, 11726-31.
47. Hunter, W. N., Brown, T., Anand, N. N., and Kennard, O. (1986) Structure of an adenine-cytosine base pair in DNA and its implications for mismatch repair, Nature 320, 552-5.
48. Brown, T., Hunter, W. N., Kneale, G., and Kennard, O. (1986) Molecular structure of the G.A base pair in DNA and its implications for the mechanism of transversion mutations, Proc. Natl. Acad. Sci. U.S.A. 83, 2402-6.
49. Boulard, Y., Cognet, J. A., and Fazakerley, G. V. (1997) Solution structure as a function of pH of two central mismatches, C-T and C-C, in the 29 to 39 K-ras gene sequence, by nuclear magnetic resonance and molecular dynamics, J. Mol. Biol. 268, 331-47.