Stationary-phase persisters to ofloxacin sustain DNA damage and require repair systems only during recovery

mBio

Volumn 6, Issue 5, 2015, Pages

  Völzing, Katherine G ^a,b   Brynildsen, Mark P ^a  

^a Princeton University   (United States)

^b EXXONMOBIL UPSTREAM RESEARCH COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; ANTIINFECTIVE AGENT; DNA LIGASE;

ARTICLE; BACTERIAL CELL; BACTERIUM CULTURE; CELL GROWTH; CELL METABOLISM; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GROWTH INHIBITION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; DRUG EFFECTS; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ANTI-BACTERIAL AGENTS; DNA DAMAGE; DNA REPAIR; DNA REPAIR ENZYMES; ESCHERICHIA COLI; OFLOXACIN;

EID: 84946600316     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00731-15     Document Type: Article

References (59)

1. Klevens RM, Edwards JR, Richards CL, Horan TC, Gaynes RP, Pollock DA, Cardo DM. 2007. Estimating health care-associated infections and deaths in U.S. Hospitals, 2002. Public Health Rep 122:160-166.
2. Scott RD, II. 2009. The direct medical costs of health care-associated infections in U.S. Hospitals and the benefits of prevention. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/HAI/pdfs/hai/Scott_CostPaper.pdf.
3. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
4. Allison KR, Brynildsen MP, Collins JJ. 2011. Heterogeneous bacterial persisters and engineering approaches to eliminate them. Curr Opin Microbiol 14:593-598. http://dx.doi.org/10.1016/j.mib.2011.09.002.
5. Fauvart M, De Groote VN, Michiels J. 2011. Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol 60:699-709. http://dx.doi.org/10.1099/jmm.0.030932-0.
6. Gefen O, Balaban NQ. 2009. The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol Rev 33:704-717. http://dx.doi.org/10.1111/j.1574-6976.2008.00156.x.
7. Levin BR, Concepción-Acevedo J, Udekwu KI. 2014. Persistence: a copacetic and parsimonious hypothesis for the existence of non-inherited resistance to antibiotics. Curr Opin Microbiol 21:18-21. http://dx.doi.org/10.1016/j.mib.2014.06.016.
8. Lewis K. 2007. Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5:48-56. http://dx.doi.org/10.1038/nrmicro1557.
9. Wiuff C, Zappala RM, Regoes RR, Garner KN, Baquero F, Levin BR. 2005. Phenotypic tolerance: antibiotic enrichment of noninherited resistance in bacterial populations. Antimicrob Agents Chemother 49: 1483-1494. http://dx.doi.org/10.1128/AAC.49.4.1483-1494.2005.
10. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622-1625. http://dx.doi.org/10.1126/science.1099390.
11. Lewis K. 2010. Persister cells. Annu Rev Microbiol 64:357-372. http://dx.doi.org/10.1146/annurev.micro.112408.134306.
12. Amato SM, Fazen CH, Henry TC, Mok WW, Orman MA, Sandvik EL, Volzing KG, Brynildsen MP. 2014. The role of metabolism in bacterial persistence. Front Microbiol 5:70. http://dx.doi.org/10.3389/fmicb.2014.00070.
13. Balaban NQ. 2011. Persistence: mechanisms for triggering and enhancing phenotypic variability. Curr Opin Genet Dev 21:768-775. http://dx.doi.org/10.1016/j.gde.2011.10.001.
14. Balaban NQ, Gerdes K, Lewis K, McKinney JD. 2013. A problem of persistence: still more questions than answers? Nat Rev Microbiol 11: 587-591. http://dx.doi.org/10.1038/nrmicro3076.
15. Grant SS, Hung DT. 2013. Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence 4:273-283. http://dx.doi.org/10.4161/viru.23987.
16. Amato SM, Orman MA, Brynildsen MP. 2013. Metabolic control of persister formation in Escherichia coli. Mol Cell 50:475-487. http://dx.doi.org/10.1016/j.molcel.2013.04.002.
17. Maisonneuve E, Gerdes K. 2014. Molecular mechanisms underlying bacterial persisters. Cell 157:539-548. http://dx.doi.org/10.1016/ j.cell.2014.02.050.
18. Maisonneuve E, Castro-Camargo M, Gerdes K. 2013. (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154:1140-1150. http://dx.doi.org/10.1016/j.cell.2013.07.048.
19. Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K. 2006. Persisters: a distinct physiological state of E. coli. BMC Microbiol 6:53. http://dx.doi.org/10.1186/1471-2180-6-53.
20. Orman MA, Brynildsen MP. 2013. Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob Agents Chemother 57: 3230-3239. http://dx.doi.org/10.1128/AAC.00243-13.
21. Hansen S, Lewis K, Vulić M. 2008. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob Agents Chemother 52:2718-2726. http://dx.doi.org/10.1128/AAC.00144-08.
22. Li Y, Zhang Y. 2007. PhoU is a persistence switch involved in persister formation and tolerance to multiple antibiotics and stresses in Escherichia coli. Antimicrob Agents Chemother 51:2092-2099. http://dx.doi.org/10.1128/AAC.00052-07.
23. Luidalepp H, Jõers A, Kaldalu N, Tenson T. 2011. Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. J Bacteriol 193:3598-3605. http://dx.doi.org/10.1128/JB.00085-11.
24. Modai J. 1999. High-dose intravenous fluoroquinolones in the treatment of severe infections. J Chemother 11:478-485. http://dx.doi.org/10.1179/joc.1999.11.6.478.
25. Drlica K, Zhao X. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61:377-392.
26. Kohanski MA, Dwyer DJ, Collins JJ. 2010. How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 8:423-435. http://dx.doi.org/10.1038/nrmicro2333.
27. Sato K, Inoue Y, Fujii T, Aoyama H, Mitsuhashi S. 1986. Antibacterial activity of ofloxacin and its mode of action. Infection 14(Suppl 4): S226-S230. http://dx.doi.org/10.1007/BF01661277.
28. Dörr T, Lewis K, Vulic´ M. 2009. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet 5:e1000760. http://dx.doi.org/10.1371/journal.pgen.1000760.
29. Dörr T, Vulic´ M, Lewis K. 2010. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol 8:e1000317. http://dx.doi.org/10.1371/journal.pbio.1000317.
30. Pennington JM, Rosenberg SM. 2007. Spontaneous DNA breakage in single living Escherichia coli cells. Nat Genet 39:797-802. http://dx.doi.org/10.1038/ng2051.
31. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K. 2004. Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 230:13-18. http://dx.doi.org/10.1016/S0378-1097(03)00856-5.
32. Roostalu J, Jõers A, Luidalepp H, Kaldalu N, Tenson T. 2008. Cell division in Escherichia coli cultures monitored at single cell resolution. BMC Microbiol 8:68. http://dx.doi.org/10.1186/1471-2180-8-68.
33. Oliver JD. 2005. The viable but nonculturable state in bacteria. J Microbiol 43:93-100.
34. Orman MA, Brynildsen MP. 2013. Establishment of a method to rapidly assay bacterial persister metabolism. Antimicrob Agents Chemother 57: 4398-4409. http://dx.doi.org/10.1128/AAC.00372-13.
35. Baharoglu Z, Mazel D. 2014. SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 38:1126-1145. http://dx.doi.org/10.1111/1574-6976.12077.
36. Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V. 2013. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41:D605-D612. http://dx.doi.org/10.1093/nar/gks1027.
37. d’Ari R. 1985. The SOS system. Biochimie 67:343-347. http://dx.doi.org/10.1016/S0300-9084(85)80077-8.
38. Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V. 2013. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41:D605-D612. http://dx.doi.org/10.1093/nar/gks1027.
39. Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Muñiz-Rascado L, García-Sotelo JS, Weiss V, Solano-Lira H, Martínez-Flores I, Medina-Rivera A, Salgado-Osorio G, Alquicira-Hernández S, Alquicira-Hernández K, López-Fuentes A, Porrón-Sotelo L, Huerta AM, Bonavides-Martínez C, Balderas-Martínez YI, Pannier L, Olvera M. 2013. RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more. Nucleic Acids Res 41:D203-D213. http://dx.doi.org/10.1093/nar/gks1201.
40. Mount DW. 1977. A mutant of Escherichia coli showing constitutive expression of the lysogenic induction and error-prone DNA repair pathways. Proc Natl Acad Sci U S A 74:300-304. http://dx.doi.org/10.1073/pnas.74.1.300.
41. Hill TM, Sharma B, Valjavec-Gratian M, Smith J. 1997. sfi-independent filamentation in Escherichia coli is lexA dependent and requiresDNAdamage for induction. J Bacteriol 179:1931-1939.
42. Yu M, Souaya J, Julin DA. 1998. The 30-kDa C-terminal domain of the RecB protein is critical for the nuclease activity, but not the helicase activity, of the RecBCD enzyme from Escherichia coli. Proc Natl Acad Sci U S A 95:981-986. http://dx.doi.org/10.1073/pnas.95.3.981.
43. Yu M, Souaya J, Julin DA. 1998. Identification of the nuclease active site in the multifunctional RecBCD enzyme by creation of a chimeric enzyme. J Mol Biol 283:797-808. http://dx.doi.org/10.1006/jmbi.1998.2127.
44. Hickson ID, Robson CN, Atkinson KE, Hutton L, Emmerson PT. 1985. Reconstitution of RecBC DNase activity from purified Escherichia coli RecB and RecC proteins. J Biol Chem 260:1224-1229.
45. Courcelle J, Hanawalt PC. 2003. RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet 37:611-646. http://dx.doi.org/10.1146/annurev.genet.37.110801.142616.
46. Whitby MC, Lloyd RG. 1995. Altered SOS induction associated with mutations in recF, recO and recR. Mol Gen Genet 246:174-179. http://dx.doi.org/10.1007/BF00294680.
47. Finch PW, Finch PW, Chambers P, Emmerson PT. 1985. Identification of the Escherichia coli recN gene product as a major SOS protein. J Bacteriol 164:653-658.
48. Meddows TR, Savory AP, Grove JI, Moore T, Lloyd RG. 2005. RecN protein and transcription factor DksA combine to promote faithful recombinational repair of DNA double-strand breaks. Mol Microbiol 57: 97-110. http://dx.doi.org/10.1111/j.1365-2958.2005.04677.x.
49. Shinagawa H, Makino K, Amemura M, Kimura S, Iwasaki H, Nakata A. 1988. Structure and regulation of the Escherichia coli ruv operon involved in DNA repair and recombination. J Bacteriol 170:4322-4329.
50. Weng MW, Zheng Y, Jasti VP, Champeil E, Tomasz M, Wang Y, Basu AK, Tang MS. 2010. Repair of mitomycin C mono-and interstrand crosslinked DNA adducts by UvrABC: a new model. Nucleic Acids Res 38: 6976-6984. http://dx.doi.org/10.1093/nar/gkq576.
51. Kim J-S, Heo P, Yang T-J, Lee K-S, Jin Y-S, Kim S-K, Shin D, Kweon D-H. 2011. Bacterial persisters tolerate antibiotics by not producing hydroxyl radicals. Biochem Biophys Res Commun 413:105-110. http://dx.doi.org/10.1016/j.bbrc.2011.08.063.
52. Wu Y, Vulic´ M, Keren I, Lewis K. 2012. Role of oxidative stress in persister tolerance. Antimicrob Agents Chemother 56:4922-4926. http://dx.doi.org/10.1128/AAC.00921-12.
53. Adams KN, Takaki K, Connolly LE, Wiedenhoft H, Winglee K, Humbert O, Edelstein PH, Cosma CL, Ramakrishnan L. 2011. Drug tolerance in replicating mycobacteria mediated by a macrophage-induced efflux mechanism. Cell 145:39-53. http://dx.doi.org/10.1016/j.cell.2011.02.022.
54. Wakamoto Y, Dhar N, Chait R, Schneider K, Signorino-Gelo F, Leibler S, McKinney JD. 2013. Dynamic persistence of antibiotic-stressed mycobacteria. Science 339:91-95. http://dx.doi.org/10.1126/science.1229858.
55. Theodore A, Lewis K, Vulic M. 2013. Tolerance of Escherichia coli to fluoroquinolone antibiotics depends on specific components of the SOS response pathway. Genetics 195:1265-1276. http://dx.doi.org/10.1534/genetics.113.152306.
56. Snyder M, Drlica K. 1979. DNA gyrase on the bacterial chromosome: DNA cleavage induced by oxolinic acid. J Mol Biol 131:287-302. http://dx.doi.org/10.1016/0022-2836(79)90077-9.
57. Lu TK, Collins JJ. 2009. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc Natl Acad Sci U S A 106: 4629-4634. http://dx.doi.org/10.1073/pnas.0800442106.
58. Allison KR, Brynildsen MP, Collins JJ. 2011. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473:216-220. http://dx.doi.org/10.1038/nature10069.
59. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. 2004. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186:8172-8180. http://dx.doi.org/10.1128/JB.186.24.8172-8180.2004.