Selective target inactivation rather than global metabolic dormancy causes antibiotic tolerance in uropathogens

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 4, 2014, Pages 2089-2097

  Goneau, Lee W ^a,b   Yeoh, Nigel S ^c   MacDonald, Kyle W ^a,b   Cadieux, Peter A ^a,d   Burton, Jeremy P ^a,b   Razvi, Hassan ^a   Reid, Gregor ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d Fanshawe College   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CIPROFLOXACIN; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); GENTAMICIN; PEPTIDOGLYCAN;

ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ANTIBIOTIC TOLERANCE; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM ISOLATION; CELL ACTIVATION; CELL INACTIVATION; CELL METABOLISM; CELL TYPE; CONTROLLED STUDY; DNA REPAIR; DNA TRANSCRIPTION; DORMANCY; DRUG CROSS TOLERANCE; DRUG SENSITIZATION; DRUG TOLERANCE; DRUG TREATMENT FAILURE; ENZYME ACTIVITY; GLOBAL METABOLIC DORMANCY; HUMAN; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG TOLERANCE; NONHUMAN; PERSISTER CELL; PRIORITY JOURNAL; RECURRENT INFECTION; STAPHYLOCOCCUS SAPROPHYTICUS; TARGET CELL; TURNOVER TIME; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI;

AMPICILLIN; ANTI-BACTERIAL AGENTS; CIPROFLOXACIN; ESCHERICHIA COLI; GENTAMICINS; MICROBIAL SENSITIVITY TESTS; STAPHYLOCOCCUS;

EID: 84896922130     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02552-13     Document Type: Article

References (45)

1. Bigger JW. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244:497-500. http://dx.doi.org/10.1016/ S0140-6736(00)74210-3.
2. Lewis K. 2010. Persister cells. Annu. Rev. Microbiol. 64:357-372. http://dx.doi.org/10.1146/annurev.micro.112408.134306.
3. Lewis K. 2007. Persister cells, dormancy and infections disease. Nat. Rev. Microbiol. 5:48-56. http://dx.doi.org/10.1038/nrmicro1557. (Pubitemid 44942303)
4. Jayaraman R. 2008. Bacterial persistence: some new insights into an old phenomenon. J. Biosci. 33:795-805. http://dx.doi.org/10.1007/s12038-008-0099-3.
5. Blango MG, Mulvey MA. 2010. Persistence of Uropathogenic Escherichia coli in the face of multiple antibiotics. Antimicrob. Agents Chemother. 54:1855-1863. http://dx.doi.org/10.1128/AAC.00014-10.
6. Keren I, Minami S, Rubin E, Lewis K. 2011. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. mBio 2:e00100-11. http://dx.doi.org/10.1128/mBio.00100-11.
7. Mulcahy LR, Burns JL, Lory S, Lewis K. 2010. Emergence of Pseudomonas aeruginosa strains producing high levels of persister cells in patients with cystic fibrosis. J. Bacteriol. 192:6191-6199. http://dx.doi.org/10.1128/JB. 01651-09.
8. 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.
9. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622-1627. http://dx.doi.org/10. 1126/science.1099390.
10. 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.
11. Kussell E, Leibler S. 2005. Phenotypic diversity, population growth, and information in fluctuating environments. Science 309:2075-2080. http://dx.doi.org/10.1126/science.1114383.
12. Wu Y, Vulić 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.
13. Tashiro Y, Kawata K, Taniuchi A, Kakinuma K, May T, Okabe S. 2012. RelE-mediated dormancy is enhanced at high cell density in Escherichia coli. J. Bacteriol. 194:1169-1176. http://dx.doi.org/10.1128/JB.06628-11.
14. Grant SS, Kaufmann BB, Chand NS, Haseley N, Hung DT. 2012. Eradication of bacterial persisters with antibiotic-generated hydroxyl radicals. Proc. Natl. Acad. Sci. U. S. A. 109:12147-12152. http://dx.doi.org/10.1073/pnas.1203735109.
15. Dörr T, Lewis K, Vulić M. 2009. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 5:e1000760. http://dx.doi.org/10.1371/journal.pgen.1000760.
16. Kwan BW, Valenta JA, Benedik MJ, Wood TK. 2013. Arrested protein synthesis increases persister-like cell formation. Antimicrob. Agents Chemother. 57:1468-1473. http://dx.doi.org/10.1128/AAC.02135-12.
17. Hong SK, Wang X, O'Connor HF, Benedik MJ, Wood TK. 2012. Bacterial persistence increases as environmental fitness decreases. Microb. Biotechnol. 5: 509-522. http://dx.doi.org/10.1111/j.1751-7915.2011.00327.x.
18. Pomeranz A, El-Khayam A, Korzets Z, Kessler OJ, Godfrey L, Katz B, Wolach B. 2000. A bioassay evaluation of the urinary antibacterial efficacy of low dose prophylactic antibiotics in children with vesicoureteral reflux. J. Urol. 164: 1070-1073. http://dx.doi.org/10.1016/S0022-5347(05)67253-9. (Pubitemid 30637577)
19. Dörr T, Vulić 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.
20. Kint CI, Verstraeten N, Fauvert M, Michiels J. 2012. New-found fundamentals of bacterial persistence. Trends. Microbiol. 20:577-585. http://dx.doi.org/10.1016/j.tim.2012.08.009.
21. Moyed HS, Bertrand KP. 1983. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 155:768-775. (Pubitemid 13048115)
22. Allison KR, Brynildsen MP, Collins JJ. 2011. Heterogenous 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.
23. Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, Cohen SN. 2004. SOS response induction by β-lactams and bacterial defense against lethality. Science 305: 1629-1631. http://dx.doi.org/10.1126/science.1101630. (Pubitemid 39296359)
24. 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.
25. Hofsteenge N, van Nimwegen E, Silander OK. 2013. Quantitative analysis of persister fractions suggest different mechanisms of formation among environmental isolates of E. coli. BMC Microbiol. 13:25. http://dx.doi.org/10. 1186/1471-2180-13-25.
26. Wood TK, Knabel SJ, Kwan BW. 2013. Bacterial persister cell formation and dormancy. Appl. Environ. Microbiol. 79:7116-7121. http://dx.doi.org/10.1128/ AEM.02636-13.
27. 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.
28. 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.
29. 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.
30. Raz R, Colodner R, Kunin CM. 2005. Who are you-Staphylococcus saprophyticus? Clin. Infect. Dis. 40:896-898. http://dx.doi.org/10.1086/428353.
31. Hooton TM, Stamm WE. 1997. Diagnosis and treatment of uncomplicated urinary tract infection. Infect. Dis. Clin. North Am. 11:551-581. http://dx.doi.org/10.1016/S0891-5520(05)70373-1. (Pubitemid 27445472)
32. Warren JW, Abrutyn E, Hebel JR, Johnson JR, Schaeffer AJ, Stamm WE. 1999. Guidelines for antimicrobial treatment of uncomplicated acute bacterial cystitis and acute pyelonephritis in women. Clin. Infect. Dis. 29:745-758. http://dx.doi.org/10.1086/520427. (Pubitemid 30256361)
33. Garofalo CK, Hooton TM, Martin SM, Stamm WE, Palermo JJ, Gordon JI, Hultgren SJ. 2007. Escherichia coli from urine of female patients with urinary tract infections is competent for intracellular bacterial community formation. Infect. Immun. 75:52-60. http://dx.doi.org/10.1128/IAI.01123-06. (Pubitemid 46047878)
34. Clinical and Laboratory Standards Institute. 2007. Performance standards for antimicrobial susceptibility testing; seventeenth informational supplement. CLSI document M100-S17. Clinical and Laboratory Standards Institute, Wayne, PA.
35. 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. (Pubitemid 38091733)
36. Grønlund H, Gerdes K. 1999. Toxin-antitoxin systems homologues with relBE of Escherichia coli plasmid P307 are ubiquitous in prokaryotes. J. Mol. Biol. 285:1401-1415. http://dx.doi.org/10.1006/jmbi.1998.2416. (Pubitemid 29060444)
37. Maisonneuve E, Shakespeare LJ, Jørgensen MG, Gerdes K. 2011. Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U. S. A. 108:13206-13211. http://dx.doi.org/10.1073/pnas.1100186108.
38. Baharoglu Z, Krin E, Mazel D. 2013. RpoS plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae. PLoS Genet. 9:e1003421. http://dx.doi.org/10.1371/journal.pgen.1003421.
39. Ramage HR, Connolly LE, Cox JS. 2009. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLoS Genet. 5:e1000767. http://dx.doi.org/10.1371/journal.pgen.1000767.
40. Lee AM, Ross CT, Zeng B, Singleton SF. 2005. A molecular target for suppression of the evolution of antibiotic resistance: inhibition of the Escherichia coli RecA protein by N6-(1-napthyl)-ADP. J. Med. Chem. 48: 5408-5411. http://dx.doi.org/10.1021/jm050113z. (Pubitemid 41209237)
41. Vega NM, Allison KR, Khalil AS, Collins JJ. 2012. Signalling-mediated bacterial persister formation. Nat. Chem. Biol. 8:431-433. http://dx.doi.org/10. 1038/nchembio.915.
42. Kohanski MA, DePristo MA, Collins JJ. 2010. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 37:311-320. http://dx.doi.org/10.1016/j.molcel.2010.01.003.
43. 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. (Pubitemid 40463380)
44. Allison KR, Brynildsen MP, Collins JJ. 2011. Metabolite-eradication of bacterial persisters by aminoglycosides. Nature 473:216-220. http://dx.doi.org/10.1038/nature10069.
45. Nickel CJ. 2005. Practical management of recurrent urinary tract infections in premenopausal women. Rev. Urol. 7:11-18.