The ε subunit of DNA polymerase III is involved in the nalidixic acid-induced SOS response in Escherichia coli

Journal of Bacteriology

Volumn 190, Issue 15, 2008, Pages 5239-5247

  Pohlhaus, Jennifer Reineke ^a   Long, David T ^a   O'Reilly, Erin ^a   Kreuzer, Kenneth N ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE EPSILON; DNA TOPOISOMERASE (ATP HYDROLYSING); DOUBLE STRANDED DNA; EXODEOXYRIBONUCLEASE V; MITOMYCIN C; NALIDIXIC ACID; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RECA PROTEIN; ANTIINFECTIVE AGENT; BETA GALACTOSIDASE; DIND PROTEIN, E COLI; DNA DIRECTED DNA POLYMERASE GAMMA; DNAQ PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CELL KILLING; CONTROLLED STUDY; COVALENT BOND; DIND GENE; DNA REPAIR; DNA STRAND BREAKAGE; DNAQ GENE; DRUG CYTOTOXICITY; DRUG MECHANISM; ENZYME SUBUNIT; ESCHERICHIA COLI; GENE DISRUPTION; GENE EXPRESSION; GENE INDUCTION; GENE INSERTION; LACZ GENE; MOLECULAR STABILITY; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; REAL TIME POLYMERASE CHAIN REACTION; RECA GENE; RECN GENE; WILD TYPE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE FUSION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PHYSIOLOGY; REPORTER GENE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANTI-BACTERIAL AGENTS; ARTIFICIAL GENE FUSION; BETA-GALACTOSIDASE; DNA POLYMERASE III; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENES, REPORTER; GENETIC COMPLEMENTATION TEST; MUTAGENESIS, INSERTIONAL; NALIDIXIC ACID; SOS RESPONSE (GENETICS);

EID: 48149100780     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00173-08     Document Type: Article

References (59)

1. Aravind, L., K. S. Makarova, and E. V. Koonin. 2000. Survey and summary: Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res. 28:3417-3432.
2. Breña-Valle, M., and J. Serment-Guerrero. 1998. SOS induction by gamma-radiation in Escherichia coli strains defective in repair and/or recombination mechanisms. Mutagenesis 13:637-641.
3. Chen, C. R., M. Malik, M. Snyder, and K. Drlica. 1996. DNA gyrase and topoisomerase IV on the bacterial chromosome: quinolone-induced DNA cleavage. J. Mol. Biol. 258:627-637.
4. Connelly, J. C., E. S. de Leau, and D. R. Leach. 2003. Nucleolytic processing of a protein-bound DNA end by the E. coli SbcCD (MR) complex. DNA Repair 2:795-807.
5. Connelly, J. C., L. A. Kirkham, and D. R. Leach. 1998. The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl. Acad. Sci. USA 95:7969-7974.
6. Cox, E. C. 1976. Bacterial mutator genes and the control of spontaneous mutation. Annu. Rev. Genet. 10:135-156.
7. Cozzarelli, N. R. 1980. DNA gyrase and the supercoiling of DNA. Science 207:953-960.
8. D'Arpa, P., C. Beardmore, and L. F. Liu. 1990. Involvement of nucleic acid synthesis in cell killing mechanisms of topoisomerase poisons. Cancer Res. 50:6919-6924.
9. D'Arpa, P., and L. Liu. 1989. Topoisomerase-targeting antitumor drugs. Biochim. Biophys. Acta 989:163-177.
10. Deitz, W. H., T. M. Cook, and W. A. Goss. 1966. Mechanism of action of nalidixic acid on Escherichia coli. III. Conditions required for lethality. J. Bacteriol. 91:768-773.
11. Drlica, K., and X. Zhao. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61:377-392.
12. Fath, M., H. Mahanty, and R. Kolter. 1989. Characterization of a purF operon mutation which affects colicin V production. J. Bacteriol. 171:3158-3161.
13. Friedberg, E., G. Walker, W. Siede, R. Wood, R. Schultz, and T. Ellenberger. 2006. DNA repair and mutagenesis, 2nd ed. ASM Press, Washington, DC.
14. Gudas, L. J., and A. B. Pardee. 1976. DNA synthesis inhibition and the induction of protein X in Escherichia coli. J. Mol. Biol. 101:459-477.
15. Heitman, J., and P. Model. 1991. SOS induction as an in vivo assay of enzyme-DNA interactions. Gene 103:1-9.
16. Hishida, T., Y.-W. Han, T. Shibata, Y. Kubota, Y. Ishino, H. Iwasaki, and H. Shinagawa. 2004. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks. Genes Dev. 18:1886-1897.
17. Holm, C., J. M. Covey, D. Kerrigan, and Y. Pommier. 1989. Differential requirement of DNA replication for the cytotoxicity of DNA topoisomerase I and II inhibitors in Chinese hamster DC3F cells. Cancer Res. 49:6365-6368.
18. Hong, G., and K. N. Kreuzer. 2003. Endonuclease cleavage of blocked replication forks: an indirect pathway of DNA damage from antitumor drug-topoisomerase complexes. Proc. Natl. Acad. Sci. USA 100:5046-5051.
19. Horiuchi, T., H. Maki, M. Maruyama, and M. Sekiguchi. 1981. Identification of the dnaQ gene product and location of the structura gene for RNase H of Escherichia coli by cloning of the genes. Proc. Natl. Acad. Sci. USA 78:3770-3774.
20. Horiuchi, T., H. Maki, and M. Sekiguchi. 1978. A new conditional lethal mutator (dnaQ49) in Escherichia coli K12. Mol. Gen. Genet. 163:277-283.
21. Lancy, E. D., M. R. Lifsics, D. G. Kehres, and R. Maurer. 1989. Isolation and characterization of mutants with deletions in dnaQ, the gene for the editing subunit of DNA polymerase III in Salmonella typhimurium. J. Bacteriol. 171:5572-5580.
22. Lancy, E. D., M. R. Lifsics, P. Munson, and R. Maurer. 1989. Nucleotide sequences of dnaE, the gene for the polymerase subunit of DNA polymerase III in Salmonella typhimurium, and a variant that facilitates growth in the absence of another polymerase subunit. J. Bacteriol. 171:5581-5586.
23. Lewin, C. S., B. M. Howard, N. T. Ratcliffe, and J. T. Smith. 1989. 4-Quinolones and the SOS response. J. Med. Microbiol. 29:139-144.
24. Lifsics, M. R., E. D. Lancy, Jr., and R. Maurer. 1992. DNA replication defect in Salmonella typhimurium mutants lacking the editing (epsilon) subunit of DNA polymerase III. J. Bacteriol. 174:6965-6973.
25. Liu, D., Y. S. Wang, and D. F. Wyss. 2003. Solution structure of the hypothetical protein YqgF from Escherichia coli reveals an RNAse H fold. J. Biomol. NMR 27:389-392.
26. Liu, L. 1983. DNA topoisomerases - enzymes that catalyze the breaking and rejoining of DNA. Crit. Rev. Biochem. 15:1-24.
27. Maki, H., T. Horiuchi, and M. Sekiguchi. 1983. Structure and expression of the dnaQ mutator and the RNase H genes of Escherichia coli: overlap of the promoter regions. Proc. Natl. Acad. Sci. USA 80:7137-7141.
28. Malik, M., X. Zhao, and K. Drlica. 2006. Lethal fragmentation of bacterial chromosomes mediated by DNA gyrase and quinolones. Mol. Microbiol. 61:810-825.
29. Marians, K. J., H. Hiasa, D. R. Kim, and C. S. McHenry. 1998. Role of the core DNA polymerase III subunits at the replication fork. Alpha is the only subunit required for processive replication. J. Biol. Chem. 273: 2452-2457.
30. McDaniel, L. S., L. H. Rogers, and W. E. Hill. 1978. Survival of recombination-deficient mutants of Escherichia coli during incubation with nalidixic acid. J. Bacteriol. 134:1195-1198.
31. McPartland, A., L. Green, and H. Echols. 1980. Control of recA gene RNA in E. coli: regulatory and signal genes. Cell 20:731-737.
32. Meddows, T. R., A. P. Savory, J. I. Grove, T. Moore, and R. G. Lloyd. 2005. RecN protein and transcription factor DksA combine to promote faithful recombinational repair of DNA double-strand breaks. Mol. Microbiol. 57: 97-110.
33. Michel, B. 2000. Replication fork arrest and DNA recombination. Trends Biochem. Sci. 25:173-178.
34. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Morag, A. S., C. J. Saveson, and S. T. Lovett. 1999. Expansion of DNA repeats in Escherichia coli: effects of recombination and replication functions. J. Mol. Biol. 289:21-27.
36. Myers, R. S., and F. W. Stahl. 1994. Chi and the RecBCD enzyme of Escherichia coli. Annu. Rev. Genet. 28:49-70.
37. Newmark, K. G., E. K. O'Reilly, J. R. Pohlhaus, and K. N. Kreuzer. 2005. Genetic analysis of the requirements for SOS induction by nalidixic acid in Escherichia coli. Gene 356:69-76.
38. Oller, A. R., I. J. Fijalkowska, and R. M. Schaaper. 1993 The Escherichia coli galK2 papulation assay: its specificity and application to seven newly isolated mutator strains. Mutat. Res. 292:175-185.
39. O'Reilly, E. K., and K. N. Kreuzer. 2004. Isolation of SOS constitutive mutants of Escherichia coli. J. Bacteriol. 186:7149-7160.
40. Picksley, S., P. Attfield, and R. Lloyd. 1984. Repair of DNA double-strand
41. breaks in Escherichia coli K12 requires a functional recN product. Mol. Gen. Genet. 195:267-274.
42. Pohlhaus, J. R., and K. N. Kreuzer. 2005. Norfloxacin-induced DNA gyrase cleavage complexes block Escherichia coli replication forks, causing double-stranded breaks in vivo. Mol. Microbiol. 56:1416-1429.
43. Robbins-Manke, J. L., Z. Z. Zdraveski, M. Marinus, and J. M. Essigmann. 2005. Analysis of global gene expression and double-strand-break formation in DNA adenine methyltransferase- and mismatch repair-deficient Escherichia coli. J. Bacteriol. 187:7027-7037.
44. Sassanfar, M., and J. W. Roberts. 1990. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J. Mol. Biol. 212: 79-96.
45. Saveson, C. J., and S. T. Lovett. 1997. Enhanced deletion formation by aberrant DNA replication in Escherichia coli. Genetics 146:457-470.
46. Scheuermann, R. H., and H. Echols. 1984. A separate editing exonuclease for DNA replication: the epsilon subunit of Escherichia coli DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. USA 81:7747-7751.
47. ts mutants require recA. Mol. Microbiol. 38:565-574.
48. Skaar, E. P., M. P. Lazio, and H. S. Seifert. 2002. Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J. Bacteriol. 184:919-927.
49. Slater, S., and R. Maurer. 1993. Simple phagemid-based system for generating allele replacements in Escherichia coli. J. Bacteriol. 175:4260-4262.
50. Slater, S. C., M. R. Lifsics, M. O'Donnell, and R. Maurer. 1994. holE, the gene coding for the theta subunit of DNA polymerase III of Escherichia coli: characterization of a holE mutant and comparison with a dnaQ (epsilon-subunit) mutant. J. Bacteriol. 176:815-821.
51. Studwell, P. S., and M. O'Donnell. 1990. Processive replication is contingent on the exonuclease subunit of DNA polymerase III holoenzyme. J. Biol. Chem. 265:1171-1178.
52. Sutton, M. D., M. F. Farrow, B. M. Burton, and G. C. Walker. 2001. Genetic interactions between the Escherichia coli umuDC gene products and the beta processivity clamp of the replicative DNA polymerase. J. Bacteriol. 183: 2897-2909.
53. Sutton, M. D., S. Murli, T. Opperman, C. Klein, and G. C. Walker. 2001. umuDC-dnaQ interaction and its implications for cell cycle regulation and SOS mutagenesis in Escherichia coli. J. Bacteriol. 183:1085-1089.
54. Sutton, M. D., B. T. Smith, V. G. Godoy, and G. C. Walker. 2000. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34:479-497.
55. Walker, G. C. 1996. The SOS response of Escherichia coli, p. 1400-1416. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, DC.
56. Wang, J. C. 2002. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3:430-440.
57. Whitby, M. C., and R. G. Lloyd. 1995. Altered SOS induction associated with mutations in recF, recO and recR. Mol. Gen. Genet. 246:174-179.
58. Wilson, W. R., and G. F. Whitmore. 1981. Cell-cycle-stage specificity of 4′-(9-acridinylamino)methanesulfon-m-anisidide (m-AMSA) and interaction with ionizing radiation in mammalian cell cultures. Radiat. Res. 87:121-136.
59. Zhao, X., M. Malik, N. Chan, A. Drlica-Wagner, J.-Y. Wang, X. Li, and K. Drlica. 2006. Lethal action of quinolones against a temperature-sensitive dnaB replication mutant of Escherichia coli. Antimicrob. Agents Chemother. 50:362-364.