Analysis of the tolerance of pathogenic enterococci and staphylococcus aureus to cell wall active antibiotics

Journal of Antimicrobial Chemotherapy

Volumn 68, Issue 9, 2013, Pages 2083-2091

  Ladjouzi, Rabia ^a,b   Bizzini, Alain ^a   Lebreton, François ^a,c   Sauvageot, Nicolas ^a   Rincé, Alain ^a   Benachour, Abdellah ^a   Hartke, Axel ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITY OF BEJAIA   (Algeria)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bactericidal antibiotics; Oxidative stress; Superoxide dismutases

Indexed keywords

AMPICILLIN; CHLORAMPHENICOL; ERYTHROMYCIN; KANAMYCIN; PENICILLIN DERIVATIVE; SUPEROXIDE DISMUTASE; TETRACYCLINE; VANCOMYCIN;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; DRUG TOLERANCE; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; ENZYME ACTIVITY; EXPRESSION VECTOR; GENE DELETION; GENETIC COMPLEMENTATION; GENETIC TRANSFORMATION; MOLECULAR CLONING; NONHUMAN; PROCEDURES; STAPHYLOCOCCUS AUREUS; WILD TYPE;

BACTERICIDAL ANTIBIOTICS; OXIDATIVE STRESS; SUPEROXIDE DISMUTASES;

ANTI-BACTERIAL AGENTS; CELL WALL; DRUG TOLERANCE; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; GENE DELETION; GENETIC COMPLEMENTATION TEST; MICROBIAL SENSITIVITY TESTS; PENICILLINS; STAPHYLOCOCCUS AUREUS; SUPEROXIDE DISMUTASE; VANCOMYCIN;

EID: 84882665708     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkt157     Document Type: Article

References (44)

1. Bumann D. Pathogen proteomes during infection: a basis for infection research and novel control strategies. J Proteomics 2010; 73: 2267-76.
2. Dubée V, Chau F, Arthur M et al. The in vitro contribution of autolysins to bacterial killing elicited by amoxicillin increases with inoculum size in Enterococcus faecalis. Antimicrob Agents Chemother 2011; 55: 910-2.
3. Tomasz A, Waks S. Mechanism of action of penicillin: triggering of the pneumococcal autolytic enzyme by inhibitors of cell wall synthesis. Proc Natl Acad Sci USA 1975; 72: 4162-6.
4. Dwyer DJ, Kohanski MA, Collins JJ. Role of reactive oxygen species in antibiotic action and resistance. Curr Opin Microbiol 2009; 12: 482-9.
5. Kohanski MA, Dwyer DJ, Hayete B et al. A commonmechanismof cellular death induced by bactericidal antibiotics. Cell 2007; 130: 797-810.
6. Dwyer DJ, Kohanski MA, Hayete B et al. Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol Syst Biol 2007; 3: 91.
7. Foti JJ, Devadoss B, Winkler JA et al. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 2012; 336: 315-9.
8. Simonsen GS, Småbrekke L, Monnet DL et al. Prevalence of resistance to ampicillin, gentamicin and vancomycin in Enterococcus faecalis and Enterococcus faecium isolates from clinical specimens and use of antimicrobials in five Nordic hospitals. J Antimicrob Chemother 2003; 51: 323-31.
9. Bizzini A, Zhao C, Auffray Y et al. The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J Antimicrob Chemother 2009; 64: 1196-202.
10. Krogstad DJ, Pargwette AR. Defective killing of enterococci: a common property of antimicrobial agents acting on the cell wall. Antimicrob Agents Chemother 1980; 17: 965-8.
11. Moellering RC Jr, Korzeniowski OM, Sande MA et al. Species-specific resistance to antimicrobial synergism in Streptococcus faecium and Streptococcus faecalis. J Infect Dis 1979; 140: 203-8.
12. Finberg RW, Moellering RC, Tally FP et al. The importance of bactericidal drugs: future directions in infectious disease. Clin Infect Dis 2004; 39: 1314-20.
13. Verneuil N, Mazé A, Sanguinetti M et al. Implication of (Mn)superoxide dismutase of Enterococcus faecalis in oxidative stress responses and survival inside macrophages. Microbiology 2006; 152: 2579-89.
14. Feld L, Knudsen GM, Gram L. Bactericidal antibiotics do not appear to cause oxidative stress in Listeria monocytogenes. Appl Environ Microbiol 2012; 78: 4353-7.
15. Wang X, Zhao X. Contribution of oxidative damage to antimicrobial lethality. Antimicrob Agents Chemother 2009; 53: 1395-402.
16. Terzaghi BE, Sandine WE. Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 1975; 29: 807-13.
17. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2001.
18. Cruz-Rodz AL, Gilmore MS. High efficiency introduction of plasmid DNA into glycine treated Enterococcus faecalis byelectroporation. Mol Gen Genet 1990; 224: 152-4.
19. Thurlow LR, Thomas VC, Hancock LE. Capsular polysaccharide production in Enterococcus faecalis and contribution of CpsF to capsule serospecificity. J Bacteriol 2009; 191: 6203-10.
20. Maguin E, Duwat P, Hege T et al. New thermosensitive plasmid for gram-positive bacteria. J Bacteriol 1992; 174: 5633-8.
21. Bryan EM, Bae T, Kleerebezem M et al. Improved vectors for nisin-controlled expression in gram-positive bacteria. Plasmid 2000; 44: 183-90.
22. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-54.
23. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-5.
24. Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 1971; 44: 276-87.
25. Bizzini A, Zhao C, Budin-Verneuil A et al. Glycerol is metabolized in a complex and strain-dependent manner in Enterococcus faecalis. J Bacteriol 2010; 192: 779-85.
26. BourgogneA, GarsinDA, Qin Xet al. Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol 2008; 9: R110.
27. McBride SM, Fischetti VA, Leblanc DJ et al. Genetic diversity among Enterococcus faecalis. PLoS One 2007; 2: e582.
28. Sahm DF, Kissinger J, Gilmore MS et al. In vitro susceptibility studies of vancomycin-resistant Enterococcus faecalis. Antimicrob Agents Chemother 1989; 33: 1588-91.
29. Albesa I, Becerra MC, Battán PC et al. Oxidative stress involved in the antibacterial action of different antibiotics. Biochem Biophys Res Commun 2004; 317: 605-9.
30. Iwen PC, Kelly DM, Linder J et al. Change in prevalence and antibiotic resistance of Enterococcus species isolated from blood cultures over an 8-year period. Antimicrob Agents Chemother 1997; 41: 494-5.
31. Treitman AN, Yarnold PR, Warren J et al. Emerging incidence of Enterococcus faecium among hospital isolates (1993 to 2002). J Clin Microbiol 2005; 43: 462-3.
32. Bozdogan B, Leclercq R. Effects of genes encoding resistance to streptogramins A and B on the activity of quinupristin-dalfopristin against Enterococcus faecium. Antimicrob Agents Chemother 1999; 43: 2720-5.
33. Valderas MW, Hart ME. Identification and characterization of a second superoxide dismutase gene (sodM) from Staphylococcus aureus. J Bacteriol 2001; 183: 3399-407.
34. Chien Y, Manna AC, Projan SJ et al. SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J Biol Chem1999; 274: 37169-76.
35. Ballal A, Manna AC. Regulation of superoxide dismutase (sod) genes by SarA in Staphylococcus aureus. J Bacteriol 2009; 191: 3301-10.
36. Kohanski MA, Dwyer DJ, Wierzbowski J et al. Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 2008; 135: 679-90.
37. Liu Y, Imlay JA. Cell death from antibiotics without the involvement of reactive oxygen species. Science 2013; 339: 1210-3.
38. KerenI, WuY, Inocencio J et al. Killingbybactericidal antibioticsdoesnot depend on reactive oxygen species. Science 2013; 339: 1213-6.
39. Huycke MM. Physiology of enterococci. In: Gilmore MS, ed. The Enterococci: Pathogenesis, Molecular Biology, Antibiotic Resistance and Infection Control. Washington, DC: ASM Press, 2002: 301-54.
40. Yagi Y, Clewell DB. Recombination-deficient mutant of Streptococcus faecalis. J Bacteriol 1980; 143: 966-70.
41. Murray BE, Singh KV, Ross RP et al. Generation of restriction map of Enterococcus faecalis OG1 and investigation of growth requirements and regions encoding biosynthetic function. J Bacteriol 1993; 175: 5216-23.
42. Palmer KL, Carniol K, Manson JM et al. High-quality draft genome sequences of 28 Enterococcus sp. isolates. J Bacteriol 2010; 192: 2469-70.
43. Horsburgh MJ, Aish JL, White IJ et al. sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 2002; 184: 5457-67.
44. Arnaud M, Chastanet A, Débarbouillé M. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 2004; 70: 6887-91.