The SOS and RpoS regulons contribute to bacterial cell robustness to genotoxic stress by synergistically regulating DNA polymerase pol II

Genetics

Volumn 206, Issue 3, 2017, Pages 1349-1360

  Dapa, Tanja ^a   Fleurier, Sébastien ^a   Bredeche, Marie Florence ^a   Matic, Ivan ^a,b  

^a INSERM   (France)

^b CNRS   (France)

Author keywords

DNA polymerase II; Escherichia coli; Mitomycin C; RpoS; SOS

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA POLYMERASE; DNA POLYMERASE IB; MITOMYCIN; REACTIVE OXYGEN METABOLITE; SIGMA FACTOR RPOS; SOS PROTEIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; MUTAGENIC AGENT; POLB PROTEIN, E COLI; SIGMA FACTOR; SIGMA FACTOR KATF PROTEIN, BACTERIA;

ARTICLE; BACTERIAL CELL; CELL GROWTH; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE INDUCTION; GENOMIC INSTABILITY; GENOTOXICITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULON; SOS RESPONSE (GENETICS); DNA DAMAGE; DRUG EFFECTS; GENETICS; METABOLISM;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DNA DAMAGE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MITOMYCIN; MUTAGENS; REACTIVE OXYGEN SPECIES; REGULON; SIGMA FACTOR; SOS RESPONSE (GENETICS);

EID: 85022020154     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.199471     Document Type: Article

References (75)

1. Ali-Osman, F., A. Rairkar, and P. Young, 1995 Formation and repair of 1,3-bis-(2-chloroethyl)-1-nitrosourea and cisplatin induced total genomic DNA interstrand crosslinks in human glioma cells. Cancer Biochem. Biophys. 14: 231-241.
2. Battesti, A., N. Majdalani, and S. Gottesman, 2011 The RpoSmediated general stress response in Escherichia coli. Annu. Rev. Microbiol. 65: 189-213.
3. Becherel, O. J., and R. Fuchs, 2001 Mechanism of DNA polymerase II-mediated frameshift mutagenesis. Proc. Natl. Acad. Sci. USA 98: 8566-8571.
4. Berardini, M., P. L. Foster, and E. Loechler, 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.
5. Bouveret, E., and A. E. Battesti, 2011 The stringent response. in Bacterial Stress Responses, edited by G. Storz, and R. Hengge. ASM Press, Washington, DC.
6. Bradner, W. T., 2001 Mitomycin C: a clinical update. Cancer Treat. Rev. 27: 35-50.
7. Bryan, S., H. Chen, Y. Sun, and R. Moses, 1988 Alternate pathways of DNA replication in Escherichia coli. Biochim. Biophys. Acta 951: 249-254.
8. Centore, R. C., R. Lestini, and S. J. Sandler, 2008 XthA (Exonuclease III) regulates loading of RecA onto DNA substrates in log phase Escherichia coli cells. Mol. Microbiol. 67: 88-101.
9. Chen, H., Y. Sun, T. Stark, W. Beattie, and R. Moses, 1990 Nucleotide sequence and deletion analysis of the polB gene of Escherichia coli. DNA Cell Biol. 9: 631-635.
10. Colis, L. C., P. Raychaudhury, and A. K. Basu, 2008 Mutational specificity of gamma-radiation-induced guanine-thymine and thymine-guanine intrastrand cross-links in mammalian cells and translesion synthesis past the guanine-thymine lesion by human DNA polymerase eta. Biochemistry 47: 8070-8079.
11. Corzett, C. H., M. F. Goodman, and S. E. Finkel, 2013 Competitive fitness during feast and famine: how SOS DNA polymerases influence physiology and evolution in Escherichia coli. Genetics 194: 409-420.
12. Cunningham, R. P., S. M. Saporito, S. G. Spitzer, and B. Weiss, 1986 Endonuclease IV (nfo) mutant of Escherichia coli. J. Bacteriol. 168: 1120-1127.
13. Datsenko, K., and B. L. Wanner, 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645.
14. Delmas, S., and I. Matic, 2006 Interplay between replication and recombination in Escherichia coli: impact of the alternative DNA polymerases. Proc. Natl. Acad. Sci. USA 103: 4564-4569.
15. Demple, B., A. Johnson, and D. Fung, 1986 Exonuclease III and endonuclease IV remove 39 blocks from DNA synthesis primers in H2O2-damaged Escherichia coli. Proc. Natl. Acad. Sci. USA 83: 7731-7735.
16. Doroshow, J. H., 1986 Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinones. Med. Sci. 83: 4514-4518.
17. Escarceller, M., J. Hicks, G. Gudmundsson, G. Trump, D. Touati et al., 1994 Involvement of Escherichia coli DNA polymerase II in response to oxidative and adaptive mutation. J. Bacteriol. 176: 6221-6228.
18. Foster, P. L., 2007 Stress-induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 42: 373-397.
19. Friedberg, E. C., G. C. Walker, W. Siede, R. D. Wood, R. A. Schultz et al., 2006 DNA Repair and Mutagenesis, Ed. 2 ASM Press, Washington, DC.
20. Frisch, R. L., Y. Su, P. C. Thornton, J. L. Gibson, S. M. Rosenberg et al., 2010 Separate DNA Pol II-and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. J. Bacteriol. 192: 4694-4700.
21. Gefter, M., I. Molineux, T. Kornberg, and H. Khorana, 1972 Deoxyribonucleic acid synthesis in cell-free extracts. 3. Catalytic properties of deoxyribonucleic acid polymerase II. J. Biol. Chem. 247: 3321-3326.
22. Gottesman, S., E. Halpern, and P. Trisler, 1981 Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J. Bacteriol. 148: 265-273.
23. Gutierrez, A., L. Laureti, S. Crussard, H. Abida, A. Rodriguez-Rojas et al., 2013 Beta-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat. Commun. 4: 1610.
24. Hébrard, M., J. Viala, S. Méresse, F. Barras, and L. Aussel, 2009 Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance. J. Bacteriol. 191: 4605-4614.
25. Hengge-Aronis, R., 1996 Regulation of gene expression during entry into stationary phase, pp. 1497-1512 in Escherichia Coli and Salmonella: Cellular and Molecular Biology, edited by F.C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, and K. B. Low et al. ASM Press, Washington, DC.
26. Hengge-Aronis, R., 2002 Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 66: 373-395.
27. Hornback, M., and R. I. Roop, 2006 The Brucella abortus xthA-1 gene product participates in base excision repair and resistance to oxidative killing but is not required for wild-type virulence in the mouse model. J. Bacteriol. 188: 1295-1300.
28. Ishino, Y., H. Iwasaki, H. Fukui, J. Mineno, I. Kato et al., 1992 Aphidicolin inhibits DNA polymerizing activity but not nucleolytic activity of Escherichia coli DNA polymerase II. Biochimie 74: 131-136.
29. Iuchi, S., and L. Weiner, 1996 Cellular and molecular physiology of Escherichia coli in the adaptation to aerobic environments. J. Biochem. 120: 1055-1063.
30. Iwasaki, H., A. Nakata, G. Walker, and H. Shinagawa, 1990 The Escherichia coli polB gene, which encodes DNA polymerase II, is regulated by the SOS system. J. Bacteriol. 172: 6268-6273.
31. Iwase, T., A. Tajima, S. Sugimoto, K. Okuda, I. Hironaka et al., 2013 A simple assay for measuring catalase activity: a visual approach. Sci. Rep. 3: 3081.
32. Jin, D. J., and C. A. Gross, 1988 Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J. Mol. Biol. 202: 45-58.
33. Kelner, M., R. Bagnell, and K. Welch, 1990 Thioureas react with superoxide radicals to yield a sulfhydryl compound. Explanation for protective effect against paraquat. J. Biol. Chem. 265: 1306-1311.
34. Khil, P. P., and R. D. Camerini-Otero, 2002 Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol. Microbiol. 44: 89-105.
35. Knippers, R., 1970 DNA polymerase II. Nature 228: 1050-1053.
36. Kornberg, T., and M. L. Gefter, 1971 Purification and DNA synthesis in cell-free extracts: properties of DNA polymerase II. Proc. Natl. Acad. Sci. USA 68: 761-764.
37. Lange, R., and R. Hengge-Aronis, 1991 Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J. Bacteriol. 173: 4474-4481.
38. Little, J. W., and D. W. Mount, 1982 The SOS regulatory system of Escherichia coli. Cell 29: 11-22.
39. Loewen, P. C., B. L. Triggs, C. S. George, and B. E. Hrabarchuk, 1985 Genetic mapping of katG, a locus that affects synthesis of the bifunctional catalase-peroxidase hydroperoxidase I in Escherichia coli. J. Bacteriol. 162: 661-667.
40. Luria, S. E., and M. Delbruck, 1943 Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491-511.
41. Maisonneuve, E., M. Castro-Camargo, and K. Gerdes, 2013 (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154: 1140-1150.
42. Mathieu, A., S. Fleurier, A. Frénoy, J. Dairou, M.-F. Bredeche et al., 2016 Discovery and function of a general core hormetic stress response in E. coli induced by sublethal concentrations of antibiotics. Cell Rep. 17: 46-57.
43. Merrikh, H., A. E. Ferrazzoli, A. Bougdour, A. Olivier-Mason, and S. T. Lovett, 2009 A DNA damage response in Escherichia coli involving the alternative sigma factor, RpoS. Proc. Natl. Acad. Sci. USA 106: 611-616.
44. Michel, B., 2005 After 30 years of study, the bacterial SOS response still surprises us. PLoS Biol. 3: 1174-1176.
45. Mukhopadhyay, S., J. P. Audia, R. N. Roy, and H. E. Schellhorn, 2000 Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol. Microbiol. 37: 371-381.
46. Murphy, K. C., K. G. Campellone, and A. R. Poteete, 2000 PCRmediated gene replacement in Escherichia coli. Gene 246: 321-330.
47. Nieminuszczy, J., and E. Grzesiuk, 2007 Bacterial DNA repair genes and their eukaryotic homologues: 3. AlkB dioxygenase and Ada methyltransferase in the direct repair of alkylated DNA. Acta Biochim. Pol. 54: 459-468.
48. Ohmori, H., E. C. Friedberg, R. P. Fuchs, M. F. Goodman, F. Hanaoka et al., 2001 The Y-family of DNA polymerases. Mol. Cell 8: 7-8.
49. Park, S., X. You, and J. A. Imlay, 2005 Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx-mutants of Escherichia coli. Proc. Natl. Acad. Sci. USA 102: 9317-9322.
50. Poklar, N., D. S. Pilch, S. J. Lippard, E. A. Redding, S. U. Dunham et al., 1996 Influence of cisplatin intrastrand crosslinking on the conformation, thermal stability, and energetics of a 20-mer DNA duplex. Proc. Natl. Acad. Sci. USA 93: 7606-7611.
51. Radman, M., 1975 SOS repair hypothesis: phenomenology of an inducible DNA repair which is accompanied by mutagenesis. Basic Life Sci. 5A: 355-367.
52. Rangarajan, S., R. Woodgate, and M. F. Goodman, 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.
53. Rudd, G. N., J. A. Hartley, and R. L. Souhami, 1995 Persistence of cisplatin-induced DNA interstrand crosslinking in peripheral blood mononuclear cells from elderly and young individuals. Cancer Chemother. Pharmacol. 35: 323-326.
54. Sahu, S. N., S. Acharya, H. Tuminaro, I. Patel, K. Dudley et al., 2003 The bacterial adaptive response gene, barA, encodes a novel conserved histidine kinase regulatory switch for adaptation and modulation. Mol. Cell. Biochem. 253: 167-177.
55. Shanmughapriya, V., S. Meenakshi, and M. Hussain Munavar, 2014 Selective alleviation of mitomycin C sensitivity in lexA3 strains of Escherichia coli demands allele specificity of rif-nal mutations: a pivotal role for rpoB87-gyrA87 mutations. PLoS One 9: e87702.
56. Shee, C., J. L. Gibson, M. C. Darrow, C. Gonzalez, and S.M. Rosenberg, 2011 Impact of a stress-inducible switch to mutagenic repair of DNA breaks on mutation in Escherichia coli. Proc. Natl. Acad. Sci. USA 108: 13659-13664.
57. Silhavy, T. J., M. L. Berman, and L. W. Enquist, 1984 Experiments with Gene Fusions. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
58. Sladek, F. M., M. M. Munn, W. D. Rupp, and P. Howard-Flanders, 1989 In vitro repair of psoralen-DNA cross-links by RecA, UvrABC, and the 59-exonuclease of DNA polymerase I. J. Biol. Chem. 264: 6755-6765.
59. Slater, S., and R. Maurer, 1993 Simple phagemid-based system for generating allele replacements in Escherichia coli. J. Bacteriol. 175: 4260-4262.
60. Storvik, K. A., and P. L. Foster, 2010 RpoS, the stress response sigma factor, plays a dual role in the regulation of Escherichia coli’s error-prone DNA polymerase IV. J. Bacteriol. 192: 3639-3644.
61. Suvarnapunya, A., H. Lagassé, and M. Stein, 2003 The role of DNA base excision repair in the pathogenesis of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 48: 549-559.
62. Szybalski, W., and V. N. Iyer, 1964 Crosslinking of DNA by Enzymatically or Chemically Activated Mitomycins and Porfiromycins, Bifunctionally “Alkylating” Antibiotics. Fed. Proc. 23: 946-957.
63. Tomasz, M., 1976 H2O2 generation during the redox cycle of mitomycin C and DNA-bound mitomycin C. Chem. Biol. Interact. 13: 89-97.
64. Tomasz, M., 1995 Mitomycin C: small, fast and deadly (but very selective). Chem. Biol. 2: 575-579.
65. Tomasz, M., and Y. Palom, 1997 The mitomycin bioreductive antitumor agents: cross-linking and alkylation of DNA as the molecular basis of their activity. Pharmacol. Ther. 76: 73-87.
66. Van Houten, B., H. Gamper, S. R. Holbrook, J. E. Hearst, and A. Sancar, 1986 Action mechanism of ABC excision nuclease on a DNA substrate containing a psoralen crosslink at a defined position. Proc. Natl. Acad. Sci. USA 83: 8077-8081.
67. Wagner, J., P. Gruz, S. R. Kim, M. Yamada, K. Matsui et al., 1999 The dinB gene encodes a novel E. coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol. Cell 4: 281-286.
68. Walker, G. C., C. J. Kenyon, A. Bagg, P. J. Langer, and W.G. Shanabruch, 1982 Mutagenesis and cellular responses to DNA damage. Natl. Cancer Inst. Monogr. 60: 257-267.
69. Wang, T. C., and K. C. Smith, 1985 Role of the umuC gene in postreplication repair in UV-irradiated Escherichia coli K-12 uvrB. Mutat. Res. 145: 107-112.
70. Weber, H., T. Polen, J. Heuveling, V. F. Wendisch, and R. Hengge, 2005 Genome-wide analysis of the general stress response network in Escherichia coli: S-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187: 1591-1603.
71. Wickner, R., B. Ginsberg, I. Berkower, and J. Hurwitz, 1972 Deoxyribonucleic acid polymerase II. of Escherichia coli. I. The purification and characterization of the enzyme. J. Biol. Chem. 247: 489-497.
72. Wu, Q., L. A. Christensen, R. J. Legerski, and K. M. Vasquez, 2005 Mismatch repair participates in error-free processing of DNA interstrand crosslinks in human cells. EMBO Rep. 6: 551-557.
73. Yu, F., and S. Pan, 1993 Effect of pH on DNA alkylation by enzyme-activated mitomycin C and porfiromycin. Mol. Pharmacol. 43: 863-869.
74. Yu, D., H. M. Ellis, E. C. Lee, N. A. Jenkins, N. G. Copeland et al., 2000 An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. USA 97: 5978-5983.
75. Zaslaver, A., A. Bren, M. Ronen, S. Itzkovitz, I. Kikoin et al., 2006 A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat. Methods 3: 623-628.