Staphylococcus aureus persisters tolerant to bactericidal antibiotics

Journal of Molecular Microbiology and Biotechnology

Volumn 22, Issue 4, 2012, Pages 235-244

  Lechner, Sabrina ^a   Lewis, Kim ^b   Bertram, Ralph ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Antibiotics; Antimicrobials; Multidrug tolerance; Persister cells; Staphylococcus aureus

Indexed keywords

BENZALKONIUM CHLORIDE; CIPROFLOXACIN; DAPTOMYCIN; PENICILLIN G; RIFAMPICIN; TOBRAMYCIN;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM CULTURE; COLONY FORMING UNIT; DRUG ISOLATION; DRUG TOLERANCE; ENRICHMENT CULTURE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHENOTYPE; STAPHYLOCOCCUS AUREUS;

ANTI-BACTERIAL AGENTS; BACTERIAL LOAD; BACTERIOLOGICAL TECHNIQUES; CELL CULTURE TECHNIQUES; COLONY COUNT, MICROBIAL; CULTURE MEDIA; DAPTOMYCIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; PHENOTYPE; SENSITIVITY AND SPECIFICITY; STAPHYLOCOCCUS AUREUS; TIME FACTORS; TOBRAMYCIN;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS; STRAWBERRY CRINKLE VIRUS;

EID: 84866179937     PISSN: 14641801     EISSN: 16602412     Source Type: Journal    
DOI: 10.1159/000342449     Document Type: Article

References (54)

1. Allison KR, Brynildsen MP, Collins JJ: Heterogeneous bacterial persisters and engineering approaches to eliminate them. Curr Opin Microbiol 2011a;14: 593-598.
2. Allison KR, Brynildsen MP, Collins JJ: Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 2011b;473: 216-220.
3. Aubry-Damon H, Soussy CJ, Courvalin P: Characterization of mutations in the rpob gene that confer rifampin resistance in Staphylococcus aureus . Antimicrob Agents Chemother 1998; 42: 2590-2594. (Pubitemid 28462898)
4. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S: Bacterial persistence as a phenotypic switch. Science 2004; 305: 1622-1625. (Pubitemid 39296357)
5. Baltch AL, Ritz WJ, Bopp LH, Michelsen P, Smith RP: Activities of daptomycin and comparative antimicrobials, singly and in combination, against extracellular and intracellular Staphylococcus aureus and its stable small-colony variant in human monocyte-derived macrophages and in broth. Antimicrob Agents Chemother 2008; 52: 1829-1833. (Pubitemid 351614679)
6. Bates DM, von Eiff C, McNamara PJ, Peters G, Yeaman MR, Bayer AS, Proctor RA: Staphylococcus aureus menD and hemB mutants are as infective as the parent strains, but the menadione biosynthetic mutant persists within the kidney. J Infect Dis 2003; 187: 1654-1661. (Pubitemid 36578972)
7. Begic D, von Eiff C, Tsuji BT: Daptomycin pharmacodynamics against Staphylococcus aureus hemB mutants displaying the small colony variant phenotype. J Antimicrob Chemother 2009; 63: 977-981.
8. Bigger J: Treatment of staphylococcal infections with penicillin. Lancet 1944; 244: 497-500.
9. Bischoff M, Entenza JM, Giachino P: Influence of a functional sigB operon on the global regulators sar and agr in Staphylococcus aureus . J Bacteriol 2001; 183: 5171-5179. (Pubitemid 32750946)
10. Bradley JJ, Mayhall CG, Dalton HP: Incidence and characteristics of antibiotic-tolerant strains of Staphylococcus aureus . Antimicrob Agents Chemother 1978; 13: 1052-1057. (Pubitemid 8355018)
11. Brooun A, Liu S, Lewis K: A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2000; 44: 640-646. (Pubitemid 30117954)
12. Chambers HF, Deleo FR: Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009; 7: 629-641.
13. Correia FF, D'Onofrio A, Rejtar T, Li L, Karger BL, Makarova K, Koonin EV, Lewis K: Kinase activity of overexpressed hipA is required for growth arrest and multidrug tolerance in Escherichia coli . J Bacteriol 2006; 188: 8360-8367. (Pubitemid 44894035)
14. Cottarel G, Wierzbowski J: Combination drugs, an emerging option for antibacterial therapy. Trends Biotechnol 2007; 25: 547-555. (Pubitemid 350138177)
15. Dhar N, McKinney JD: Microbial phenotypic heterogeneity and antibiotic tolerance. Curr Opin Microbiol 2007; 10: 30-38. (Pubitemid 46216877)
16. Donegan NP, Cheung AL: Regulation of the mazEF toxin-antitoxin module in Staphylococcus aureus and its impact on sigB expression. J Bacteriol 2009; 191: 2795-2805.
17. Dörr T, Lewis K, Vulic M: SOS response induces persistence to fluoroquinolones in Escherichia coli . PLoS Genet 2009; 5:e1000760.
18. Fu Z, Tamber S, Memmi G, Donegan NP, Cheung AL: Overexpression of m azFs a in S taphylococcus aureus induces bacteriostasis by selectively targeting mRNAs for cleavage. J Bacteriol 2009; 191: 2051-2059.
19. Gaupp R, Schlag S, Liebeke M, Lalk M, Götz F: Advantage of upregulation of succinate dehydrogenase in Staphylococcus aureus biofilms. J Bacteriol 2010; 192: 2385-2394.
20. Giachino P, Engelmann S, Bischoff M: Sigma(B) activity depends on rsbU in Staphylococcus aureus . J Bacteriol 2001; 183: 1843-1852. (Pubitemid 32225979)
21. Gunnison JB, Fraher MA, Jawetz E: Persistence of Staphylococcus aureus in penicillin in vitro. J Gen Microbiol 1964; 35: 335-349.
22. Harrison JJ, Turner RJ, Ceri H: Persister cells, the biofilm matrix and tolerance to metal cations in biofilm and planktonic Pseudomonas aeruginosa . Environ Microbiol 2005; 7: 981-994. (Pubitemid 40817155)
23. Herbert S, Ziebandt AK, Ohlsen K, Schäfer T, Hecker M, Albrecht D, Novick R, Götz F: Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun 2010; 78: 2877-2889.
24. Iordanescu S, Surdeanu M: Two restriction and modification systems in Staphylococcus aureus NCTC8325. J Gen Microbiol 1976; 96: 277-281.
25. Keren I, Kaldalu N, Spoering A, Wang Y, Lewis K: Persister cells and tolerance to antimicrobials. FEMS Microbiol Lett 2004a;230: 13-18. (Pubitemid 38091733)
26. Keren I, Minami S, Rubin E, Lewis K: Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. mBio 2011; 2:e00100-e00111.
27. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K: Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli . J Bacteriol 2004b;186: 8172-8180. (Pubitemid 39603206)
28. Kim JS, Heo P, Yang TJ, Lee KS, Cho DH, Kim BT, Suh JH, Lim HJ, Shin D, Kim SK, Kweon DH: Selective killing of bacterial persisters by a single chemical compound without affecting normal antibiotic-sensitive cells. Antimicrob Agents Chemother 2011; 55: 5380-5383.
29. Lafleur MD, Qi Q, Lewis K: Patients with longterm oral carriage harbor high-persister mutants of Candida albicans . Antimicrob Agents Chemother 2010; 54: 39-44.
30. Lewis K: Persister cells, dormancy and infectious disease. Nat Rev Microbiol 2007; 5: 48-56. (Pubitemid 44942303)
31. Lewis K: Persister cells. Annu Rev Microbiol 2010a;64: 357-372.
32. Lewis K: Persister cells and the paradox of chronic infections. Microbe 2010b;5: 429-437.
33. Mascio CT, Alder JD, Silverman JA: Bactericidal action of daptomycin against stationaryphase and nondividing Staphylococcus aureus cells. Antimicrob Agents Chemother 2007; 51: 4255-4260. (Pubitemid 350209874)
34. Mayhall CG, Medoff G, Marr JJ: Variation in the susceptibility of strains of Staphylococcus aureus to oxacillin, cephalothin, and gentamicin. Antimicrob Agents Chemother 1976; 10: 707-712.
35. Möker N, Dean CR, Tao J: Pseudomonas aeruginosa increases formation of multidrug-tolerant persister cells in response to quorumsensing signaling molecules. J Bacteriol 2010; 192: 1946-1955.
36. Moyed HS, Bertrand KP: HipA , a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol 1983; 155: 768-775. (Pubitemid 13048115)
37. Moyed HS, Broderick SH: 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 1986; 166: 399-403. (Pubitemid 16112134)
38. Newsom SW: Staphylococcal persisters grown from empyema fluid on L-form medium. J Med Microbiol 1970; 3: 669-673.
39. Novick R: Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus . Virology 1967; 33: 155-166.
40. Novick RP, Geisinger E: Quorum sensing in staphylococci. Annu Rev Genet 2008; 42: 541-564.
41. Proctor RA, von Eiff C, Kahl BC, Becker K, Mc-Namara P, Herrmann M, Peters G: Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections. Nat Rev Microbiol 2006; 4: 295-305.
42. Scherrer R, Moyed HS: Conditional impairment of cell division and altered lethality in hipA mutants of Escherichia coli K-12. J Bacteriol 1988; 170: 3321-3326.
43. Senn MM, Giachino P, Homerova D, Steinhuber A, Strassner J, Kormanec J, Flückiger U, Berger-Bächi B, Bischoff M: Molecular analysis and organization of the, B operon in Staphylococcus aureus . J Bacteriol 2005; 187: 8006-8019. (Pubitemid 41691694)
44. Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K: Persisters: a distinct physiological state of E. coli . BMC Microbiol 2006; 6: 53.
45. Shapiro JA, Nguyen VL, Chamberlain NR: Evidence for persisters in Staphylococcus epidermidis RP62A planktonic cultures and biofilms. J Med Microbiol 2011; 60: 950-960.
46. Singh R, Ray P, Das A, Sharma M: Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J Med Microbiol 2009; 58: 1067-1073.
47. Spoering AL, Lewis K: Biofilms and planktonic cells of Pseudomonas aeruginosa have similar resistance to killing by antimicrobials. J Bacteriol 2001; 183: 6746-6751. (Pubitemid 33064186)
48. Steenbergen JN, Alder J, Thorne GM, Tally FP: Daptomycin: a lipopeptide antibiotic for the treatment of serious gram-positive infections. J Antimicrob Chemother 2005; 55: 283-288. (Pubitemid 40425449)
49. Tuchscherr L, Medina E, Hussain M, Völker W, Heitmann V, Niemann S, Holzinger D, Roth J, Proctor RA, Becker K, Peters G, Löffler B: Staphylococcus aureus phenotype switching: an effective bacterial strategy to escape host immune response and establish a chronic infection. EMBO Mol Med 2011; 3: 129-141.
50. Vazquez-Laslop N, Lee H, Neyfakh AA: Increased persistence in Escherichia coli caused by controlled expression of toxins or other unrelated proteins. J Bacteriol 2006; 188: 3494-3497. (Pubitemid 43726213)
51. Vega NM, Allison KR, Khalil AS, Collins JJ: Signaling-mediated bacterial persister formation. Nat Chem Biol 2012; 8: 431-433.
52. von Eiff C: Staphylococcus aureus small colony variants: a challenge to microbiologists and clinicians. Int J Antimicrob Agents 2008; 31: 507-510.
53. von Eiff C, Heilmann C, Proctor RA, Wolz C, Peters G, Götz F: A site-directed Staphylococcus aureus hemB mutant is a small-colony variant which persists intracellularly. J Bacteriol 1997; 179: 4706-4712. (Pubitemid 27339714)
54. Wiuff C, Zappala RM, Regoes RR, Garner KN, Baquero F, Levin BR: Phenotypic tolerance: antibiotic enrichment of noninherited resistance in bacterial populations. Antimicrob Agents Chemother 2005; 49: 1483-1494. (Pubitemid 40463380)