DNA polymerase II as a fidelity factor in chromosomal DNA synthesis in Escherichia coli

Molecular Microbiology

Volumn 58, Issue 1, 2005, Pages 61-70

  Banach Orlowska, Magdalena ^a   Fijalkowska, Iwona J ^a   Schaaper, Roel M ^b   Jonczyk, Piotr ^a  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

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

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA;

ALLELE; ARTICLE; BACTERIAL STRAIN; CHROMOSOME REPLICATION; DNA STRAND; DNA SYNTHESIS; ESCHERICHIA COLI; GENE INSERTION; GENE MUTATION; GENE REPLICATION; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL;

ALLELES; BETA-GALACTOSIDASE; BINDING, COMPETITIVE; CHROMOSOMES, BACTERIAL; DNA POLYMERASE II; DNA POLYMERASE III; DNA REPAIR ENZYMES; DNA REPLICATION; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENES, BACTERIAL; GENES, REPORTER; MUTATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 26244456365     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04805.x     Document Type: Article

References (58)

1. Berardini, M., Foster, P.L., and Loechler, E.L. (1999) DNA polymerase II (polB) is involved in a new DNA repair pathway for DNA interstrand cross-links in Escherichia coli. J Bacteriol 181: 2878-2882.
2. Berlyn, M.K. (1998) Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Rev 54:130-197.
3. Bonner, C.A., Hays, S., McEntee, K., and Goodman, M.F. (1990) DNA polymerase II is encoded by the DNA damage-inducible dinA gene of Escherichia coli. Proc Natl Acad Sci USA 87: 7663-7667.
4. Bonner, C.A., Stukenberg, P.T., Rajagopalan, M., Eritja, R., O'Donnell, M., McEntee, K., et al. (1992) Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins. J Biol Chem 267: 11431-11438.
5. Cai, H., Yu, H., McEntee, K., Kunkel, T.A., and Goodman, M.F. (1995) Purification and properties of wild-type and exonuclease-deficient DNA polymerase II from Escherichia coli. J Biol Chem 270: 15327-15335.
6. Cox, M.M., Goodman, M.F., Kreuzer, K.N., Sherratt, D.J., Sandler, S.J., and Marians, K.J. (2000) The importance of repairing stalled replication forks. Nature 404: 37-41.
7. Cupples, C.G., and Miller, J.H. (1989) A set of lacZ mutations in Escherichia coli that allow rapid detection of each of the six base substitutions. Proc Natl Acad Sci USA 86: 5345-5349.
8. Escarceller, M., Hicks, J., Gudmundsson, G., Trump, G., Touati, D., Lovett, S., et al. (1994) Involvement of Escherichia coli DNA polymerase II in response to oxidative damage and adaptive mutation. J Bacteriol 176: 6221-6228.
9. Fijalkowska, I.J., and Schaaper, R.M. (1993) Antimutator mutations in the alpha subunit of Escherichia coli DNA polymerase III: identification of the responsible mutations and alignment with other DNA polymerases. Genetics 134: 1039-1044.
10. Fijalkowska, I.J., and Schaaper, R.M. (1995) Effects of Escherichia coli DNA antimutator alleles in a proofreading-deficient mutD5 strain. J Bacteriol 177: 5979-5986.
11. Fijalkowska, I.J., Dunn, R.L., and Schaaper, R.M. (1993) Mutants of Escherichia coli with increased fidelity of DNA replication. Genetics 134: 1023-1030.
12. Fijalkowska, I.J., Dunn, R.L., and Schaaper, R.M. (1997) Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J Bacteriol 179: 7435-7445.
13. Fijalkowska, I.J., Jonczyk, P., Maliszewska-Tkaczyk, M., Bialoskorska, M., and Schaaper, R.M. (1998) Unequal fidelity of leading and lagging strand DNA replication on the Escherichia coli chromosome. Proc Natl Acad Sci USA 95: 10020-10025.
14. Foster, P.L. (2000) Adaptive mutation in Escherichia coli. Cold Spring Harbor Symp Quant Biol 65: 21-29.
15. Foster, P.L., Gudmundsson, G., Trimarchi, J.M., Cai, H., and Goodman, M.F. (1995) Proofreading-defective DNA polymerase II increases adaptive mutation in Escherichia coli. Proc Natl Acad Sci USA 92: 7951-7955.
16. Gawel, D., Maliszewska-Tkaczyk, M., Jonczyk, P., Schaaper, R.M., and Fijalkowska, I.J. (2002) Lack of strand bias in UV-induced mutagenesis in Escherichia coli. J Bacteriol 184: 4449-4454.
17. Goodman, M.F. (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Annu Rev Biochem 70:17-50.
18. Hughes, A.J., Bryan, S.K., Chen, H., Moses, R.E., and McHenry, C.S. (1991) Escherichia coli DNA polymerase II is stimulated by DNA polymerase III holoenzyme auxiliary subunits. J Biol Chem 266: 4568-4573.
19. Ichikawa-Ryo, H., and Kondo, S. (1975) Indirect mutagenesis in phage ëby ultraviolet pre-irradiation of host bacteria. J Mol Biol 97: 77-92.
20. Iwasaki, H., Nakata, A., Walker, G.G., and Shinagawa, H. (1990) The Escherichia coli polB gene, which encodes DNA polymerase II, is regulated by the SOS system. J Bacteriol 172: 6268-6273.
21. Johnson, K.A. (1993) Conformational coupling in DNA polymerase fidelity. Annu Rev Biochem 62: 685-713.
22. Kelman, Z., and O'Donnell, M. (1995) DNA polymerase III holoenzyme: structure and function of a chromosomal replication machine. Annu Rev Biochem 64: 171-200.
23. Kim, S.R., Maenhaut-Michel, G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., et al. (1997) Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci USA 94:13792-13797.
24. Kim, S.-R., Matsui, K., Yamada, P., Gruz, P., and Nohmi, T. (2001) Roles of chromosomal and episomal dinB genes encoding Pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol Genet Genom 266: 207-215.
25. Knippers, R. (1970) DNA polymerase II. Nature (London) 228: 1050-1053.
26. Kornberg, A., and Baker, T.A. (1992) DNA Replication, 2nd edn. New York: Freeman.
27. Kuban, W., Jonczyk, P., Gawel, D., Malanowska, K., Schaaper, R.M., and Fijalkowska, I.J. (2004) Role of Escherichia coli DNA polymerase IV in in vivo replication fidelity. J Bacteriol 186: 4802-4807.
28. Leu, F.P., Georgescu, R., and O'Donnell, M. (2003) Mechanism of the E. coli tau processivity switch during lagging-strand synthesis. Mol Cell 11: 315-327.
29. McHenry, C.S. (2003) Chromosomal replicases as asymmetric dimers: studies of subunit arrangement and functional consequences. Mol Microbiol 49: 1157-1165.
30. McInerney, P., and O'Donnell, M. (2004) Functional uncoupling of twin polymerases. Mechanism of polymerase dissociation from a lagging strand block. J Biol Chem 279: 21543-21551.
31. McKenzie, G.J., Lee, P.L., Lombardo, M.-J., Hastings, P.J., and Rosenberg, S.M. (2001) SOS mutator DNA polymerase IV functions in adaptive mutation and not adaptive amplification. Mol Cell 7: 571-579.
32. Erratum: Mol Cell 7: 1119.
33. Maliszewska-Tkaczyk, M., Jonczyk, P., Bialoskorska, M., Schaaper, R.M., and Fijalkowska, I.J. (2000) SOS mutator activity: unequal mutagenesis on leading and lagging strands. Proc Natl Acad Sci USA 97: 12678-12683.
34. Masker, W., Hanawalt, P., and Shizuya, H. (1973) Role of DNA polymerase II in repair replication in Escherichia coli. Nat New Biol 244: 242-243.
35. Mo, J.Y., and Schaaper, R.M. (1996) Fidelity and error specificity of the alpha catalytic subunit of Escherichia coli DNA polymerase III. J Biol Chem 271: 18947-18953.
36. Napolitano, R., Janel-Bintz, R., Wagner, J., and Fuchs, R.P.P. (2000) All three SOS-inducible DNA polymerases (Pol II, Pol IV, and Pol V) are involved in induced mutagenesis. EMBO J 19: 6259-6265.
37. Nowosielska, A., Janion, C., and Grzesiuk, E. (2004) Effect of deletion of SOS-induced polymerases, pol II, IV, and V, on spontaneous mutagenesis in Escherichia coli mutD5. Environ Mol Mutagen 43: 226-234.
38. O'Donnell, M., Jeruzalemi, D., and Kuriyan, J. (2001) Clamp loader structure predicts the architecture of DNA polymerase III holoenzyme and RFC. Curr Biol 11: R935-R946.
39. Pavlov, Y.I., Maki, S., Maki, H., and Kunkel, T.A. (2004) Evidence for interplay among yeast replicative polymerases alpha, delta and epsilon from studies of exonuclease and polymerase active site mutations. BMC Biol 2: 11.
40. Pham, P.T., Olson, M.W., McHenry, C.S., and Schaaper, R.M. (1998) The base substitution and frameshift fidelity of Escherichia coli DNA polymerase III holoenzyme in vitro. J Biol Chem 273: 23575-23584.
41. Pham, P.T., Olson, M.W., McHenry, C.S., and Schaaper, R.M. (1999) Mismatch extension by Escherichia coli DNA polymerase III holoenzyme. J Biol Chem 274: 3705-3710.
42. Qui, Z., and Goodman, M.F. (1997) The Escherichia coli polB locus is identical to dinA, the structural gene for DNA polymerase II. Characterization of Pol II purified from a polB mutant. J Biol Chem 272: 8611-8617.
43. Rangarajan, S., Gudmundsson, G., Qiu, Z., Foster, P.L., and Goodman, M.F. (1997) Escherichia coli DNA polymerase II catalyzes chromosomal and episomal DNA synthesis in vivo. Proc Natl Acad Sci USA 94: 946-951.
44. Rangarajan, S., Woodgate, R., and Goodman, M.F. (1999) A phenotype for enigmatic DNA polymerase II: a pivotal role for pol II in replication restart in UV-irradiated Escherichia coli. Proc Natl Acad Sci USA 96: 9224-9229.
45. Reuven, N.B., Arad, G., Maor-Shoshani, A., and Livneh, Z. (1999) The mutagenesis protein UmuC is a DNA polymerase activated by UmuD', RecA, and SSB and is specialized for translesion replication. J Biol Chem 274: 31763-31766.
46. Schaaper, P.M. (1993a) The mutational specificity of two Escherichia coli dnaE antimutator alleles as determined from lacl mutation spectra. Genetics 134: 1031-1038.
47. Schaaper, R.M. (1993b) Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli. J Biol Chem 268: 23762-23765.
48. Sokal, R.R., and Rohlf, F.J. (1981) Biometry, 2nd edn. San Francisco, CA: Freeman.
49. Stukenberg, P.T., Turner, J., and O'Donnell, M. (1994) An explanation for lagging strand replication: polymerase hopping among DNA sliding clamps. Cell 78: 877-887.
50. Taft-Benz, S.A., and Schaaper, R.M. (1998) Mutational analysis of the 3'->5' proofreading exonuclease of Escherichia coli DNA polymerase III. Nucleic Acids Res 26: 4005-4011.
51. Taft-Benz, S.A., and Schaaper, R.M. (2004) The θ subunit of Escherichia coli DNA polymerase III: a role in stabilizing the epsilon proofreading subunit. J Bacteriol 186: 2774-2780.
52. Tang, M., Shen, X., Frank, E.G., O'Donnell, M., Woodgate, R., and Goodman, M.F. (1999) UmuD'(2)C is an error-prone DNA polymerase, Escherichia coli pol V. Proc Natl Acad Sci USA 96: 8919-8924.
53. Tessman, I., and Kennedy, M.A. (1994) DNA polymerase II of Escherichia coli in the bypass of abasic sites in vivo. Genetics 136: 439-448.
54. Vandewiele, D., Fernandez de Henestrosa, A.R., Timms, A.R., Bridges, B.A., and Woodgate, R. (2002) Sequence analysis and phenotypes of five temperature sensitive mutator alleles of dnaE, encoding modified alpha-catalytic subunits of Escherichia coli DNA polymerase III holoenzyme. Mutat Res 499: 85-95.
55. Wagner, J., Gruz, P., Kim, S.-R., Yamada, M., Matsui, K., Fuchs, R.P.P., and Nohmi, T. (1999) The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol Cell 4: 281-286.
56. Wickner, S., and Hurwitz, J. (1974) Conversion of φX174 viral DNA to double-stranded form by purified Escherichia coli proteins. Proc Natl Acad Sci USA 71: 4120-4124.
57. Wolff, E., Kim, M., Hu, K., Yang, H., and Miller, J.H. (2004) Polymerases leave fingerprints: analysis of the mutational spectrum in Escherichia coli rpoB to assess the role of polymerase IV in spontaneous mutation. J Bacteriol 186: 2900-2905.
58. Yeiser, B., Pepper, E.D., Goodman, M.F., and Finkel, S.E. (2002) SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness. Proc Natl Acad Sci USA 99: 8737-8741.