Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli

Journal of Bacteriology

Volumn 186, Issue 24, 2004, Pages 8172-8180

  Keren, Iris ^a   Shah, Devang ^a   Spoering, Amy ^a   Kaldalu, Niilo ^a,b   Lewis, Kim ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

^b UNIVERSITY OF TARTU   (Estonia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGLYCOSIDE ANTIBIOTIC AGENT; AMPICILLIN; ANTIBIOTIC AGENT; ANTITOXIN; BACTERICIDE; CEFOTAXIME; MITOMYCIN C; PEPTIDE DERIVATIVE; PROTEIN HIPA; PROTEIN RELE; TOBRAMYCIN; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIOFILM; CELL FUNCTION; CELL SURVIVAL; CYTOLYSIS; DRUG TARGETING; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; LETHAL GENE; MULTIDRUG RESISTANCE; NONHUMAN; PERSISTER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSLATION; VALIDATION PROCESS;

ANTI-BACTERIAL AGENTS; BIOFILMS; COLONY COUNT, MICROBIAL; CULTURE MEDIA; DNA-BINDING PROTEINS; DRUG TOLERANCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION PROFILING; MICROBIAL SENSITIVITY TESTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 10044266575     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.24.8172-8180.2004     Document Type: Article

References (51)

1. Anderl, J. N., M. J. Franklin, and P. S. Stewart. 2000. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob. Agents Chemother. 44:1818-1824.
2. Anderson, G. G., J. J. Palermo, J. D. Schilling, R. Roth, J. Heuser, and S. J. Hultgren. 2003. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301:105-107.
3. Balaban, N. Q., J. Merrin, R. Chait, L. Kowalik, and S. Leibler. 2004. Bacterial persistence as a phenotypic switch. Science 305:1622-1625.
4. Bayles, K. W. 2000. The bactericidal action of penicillin: new clues to an unsolved mystery. Trends Microbiol. 8:274-278.
5. Bigger, J. W. 1944. Treatment of staphylococcal infections with penicillin. Lancet ii:497-500.
6. Black, D. S., B. Irwin, and H. S. Moyed. 1994. Autoregulation of hip, an operon that affects lethality due to inhibition of peptidoglycan or DNA synthesis. J. Bacteriol. 176:4081-4091.
7. Black, D. S., A. J. Kelly, M. J. Mardis, and H. S. Moyed. 1991. Structure and organization of hip, an operon that affects lethality due to inhibition of peptidoglycan or DNA synthesis. J. Bacteriol. 173:5732-5739.
8. Bogosian, G., and E. V. Bourneuf. 2001. A matter of bacterial life and death. EMBO Rep. 2:770-774.
9. Brooun, A., S. Liu, and K. Lewis. 2000. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 44:640-646.
10. Brown, J. M., and K. J. Shaw. 2003. A novel family of Escherichia coli toxin-antitoxin gene pairs. J. Bacteriol. 185:6600-6608.
11. Christensen, S. K., and K. Gerdes. 2004. Delayed-relaxed response explained by hyperactivation of ReE. Mol. Microbiol. 53:587-597.
12. Christensen, S. K., M. Mikkelsen, K. Pedersen, and K. Gerdes. 2001. RelE, a global inhibitor of translation, is activated during nutritional stress. Proc. Natl. Acad. Sci. USA 98:14328-14333.
13. Christensen, S. K., K. Pedersen, F. G. Hansen, and K. Gerdes. 2003. Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J. Mol. Biol. 332:809-819.
14. Colwell, R. R., and D. J. Grimes. 2000. Nonculturable microorganisms in the environment. American Society for Microbiology, Washington, D.C.
15. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
16. Costerton, W., R. Veeh, M. Shirtliff, M. Pasmore, C. Post, and G. Ehrlich. 2003. The application of biofilm science to the study and control of chronic bacterial infections. J. Clin. Investig. 112:1466-1477.
17. Datsenko, K. A., 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.
18. Drenkard, E., and F. M. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740-743.
19. Falla, T. J., and I. Chopra. 1998. Joint tolerance to beta-lactam and fluoroquinolone antibiotics in Escherichia coli results from overexpression of hipA. Antimicrob. Agents Chemother. 42:3282-3284.
20. Falla, T. J., and I. Chopra. 1999. Stabilization of Rhizobium symbiosis plasmids. Microbiology 145:515-516.
21. Gerdes, K., P. B. Rasmussen, and S. Molin. 1986. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc. Natl. Acad. Sci. USA 83:3116-3120.
22. Gilbert, P., P. J. Collier, and M. R. Brown. 1990. Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob. Agents Chemother. 34:1865-1868.
23. Hayes, F. 2003. Toxins-antitoxins: plasmid maintenance, programmed cell death, and cell cycle arrest. Science 301:1496-1499.
24. Hazan, R., B. Sat, and H. Engelberg-Kulka. 2004. Escherichia coli mazEF-mediated cell death is triggered by various stressful conditions. J. Bacteriol. 186:3663-3669.
25. Hsieh, P. C., S. A. Siegel, B. Rogers, D. Davis, and K. Lewis. 1998. Bacteria lacking a multidrug pump: a sensitive tool for drug discovery. Proc. Natl. Acad. Sci. USA 95:6602-6606.
26. Kaeberlein, T., K. Lewis, and S. S. Epstein. 2002. Isolating "uncultivable" microorganisms in pure culture in a simulated natural environment. Science 296:1127-1129.
27. Kaldalu, N., R. Mei, and K. Lewis. 2004. Killing by ampicillin and ofloxacin induces overlapping changes in Escherichia coli transcription profile. Antimicrob. Agents Chemother. 48:890-896.
28. Keren, I., N. Kaldalu, A. Spoering, Y. Wang, and K. Lewis. 2004. Persister cells and tolerance to antimicrobials. FEMS Microbiol. Lett. 230:13-18.
29. Korch, S. B., T. A. Henderson, and T. M. Hill. 2003. Characterization of the hipA7 allele of Escherichia coli and evidence that high persistence is governed by (p)ppGpp synthesis. Mol. Microbiol. 50:1199-1213.
30. Korobkova, E., T. Emonet, J. M. Vilar, T. S. Shimizu, and P. Cluzel. 2004. From molecular noise to behavioural variability in a single bacterium. Nature 428:574-578.
31. Lewis, K. 2000. Programmed death in bacteria. Microbiol. Mol. Biol. Rev. 64:503-514.
32. Lewis, K. 2001. Riddle of biofilm resistance. Antimicrob. Agents Chemother. 45:999-1007.
33. Mah, T. F., B. Pitts, B. Pellock, G. C. Walker, P. S. Stewart, and G. A. O'Toole. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306-310.
34. Moyed, H. S., and K. P. Bertrand. 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.
35. Moyed, H. S., and S. H. Broderick. 1986. Molecular cloning and expression of hipA, a gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J. Bacteriol. 166:399-403.
36. Opperman, T., S. Murli, B. T. Smith, and G. C. Walker. 1999. A model for a umuDC-dependent prokaryotic DNA damage checkpoint. Proc. Natl. Acad. Sci. USA 96:9218-9223.
37. Parsek, M. R., and P. K. Singh. 2003. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701.
38. Pedersen, K., S. K. Christensen, and K. Gerdes. 2002. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol. Microbiol. 45:501-510.
39. Pedersen, K., A. V. Zavialov, M. Y. Pavlov, J. Elf, K. Gerdes, and M. Ehrenberg. 2003. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112:131-140.
40. Rosenow, C., R. M. Saxena, M. Durst, and T. R. Gingeras. 2001. Prokaryotic RNA preparation methods useful for high density array analysis: comparison of two approaches. Nucleic Acids Res. 29:e112.
41. Sat, B., R. Hazan, T. Fisher, H. Khaner, G. Glaser, and H. Engelberg-Kulka. 2001. Programmed cell death in Escherichia coli: some antibiotics can trigger mazEF lethality. J. Bacteriol. 183:2041-2045.
42. Scherrer, R., and H. S. Moyed. 1988. Conditional impairment of cell division and altered lethality in hipA mutants of Escherichia coli K-12. J. Bacteriol. 170:3321-3326.
43. Selinger, D. W., K. J. Cheung, R. Mei, E. M. Johansson, C. S. Richmond, F. R. Blattner, D. J. Lockhart, and G. M. Church. 2000. RNA expression analysis using a 30 base pair resolution Escherichia coli genome array. Nat. Biotechnol. 18:1262-1268.
44. Spoering, A. L., and K. Lewis. 2001. Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J. Bacteriol. 183:6746-6751.
45. Spudich, J. L., and D. E. Koshland, Jr. 1976. Non-genetic individuality: chance in the single cell. Nature 262:467-471.
46. Tufariello, J. M., J. Chan, and J. L. Flynn. 2003. Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect. Dis. 3:578-590.
47. Tuomanen, E., and A. Tomasz. 1990. Mechanism of phenotypic tolerance of nongrowing pneumococci to beta-lactam antibiotics. Scand. J. Infect. Dis. Suppl. 74:102-112.
48. Wada, A. 1998. Growth phase coupled modulation of Escherichia coli ribosomes. Genes Cells 3:203-208.
49. 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. ASM Press, Washington, D.C.
50. Wolfson, J. S., D. C. Hooper, G. L. McHugh, M. A. Bozza, and M. N. Swartz. 1990. Mutants of Escherichia coli K-12 exhibiting reduced killing by both quinolone and β-lactam antimicrobial agents. Antimicrob. Agents Chemother. 34:1938-1943.
51. Xu, K. D., G. A. McFeters, and P. S. Stewart. 2000. Biofilm resistance to antimicrobial agents. Microbiology 146:547-549.