The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin

Journal of Antimicrobial Chemotherapy

Volumn 64, Issue 6, 2009, Pages

  Bizzini, Alain ^b   Zhao, Chen ^a   Auffray, Yanick ^a   Hartke, Axel ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Bactericidal effect; Oxidative stress; Reactive oxygen species

Indexed keywords

HYDROGEN PEROXIDE; PENICILLIN G; SUPEROXIDE; SUPEROXIDE DISMUTASE; VANCOMYCIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PENICILLIN DERIVATIVE; SODA PROTEIN, BACTERIA;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM CULTURE; BACTERIUM MUTANT; COLONY FORMING UNIT; CONTROLLED STUDY; DELETION MUTANT; DRUG EXPOSURE; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; GENETIC COMPLEMENTATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN FUNCTION; WILD TYPE; BACTERIAL COUNT; BIOLOGICAL MODEL; DRUG EFFECT; ENZYMOLOGY; GENE DELETION; GENETICS; HUMAN; MICROBIAL VIABILITY; MICROBIOLOGICAL EXAMINATION; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; COLONY COUNT, MICROBIAL; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS FAECALIS; GENE DELETION; HUMANS; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MODELS, BIOLOGICAL; PENICILLINS; SUPEROXIDE DISMUTASE; SUPEROXIDES; VANCOMYCIN;

EID: 76249086967     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkp369     Document Type: Article

References (52)

1. Murray BE. The life and times of the Enterococcus. Clin Microbiol Rev 1990; 3: 46-65.
2. Gilmore MS, Coburn PS, Nallapareddy SR et al. Enterococcal virulence. In: Gilmore MS, ed. The Enterococci: Pathogenesis, Molecular Biology, Antibiotic Resistance and Infection Control. Washington, DC, USA: ASM Press, 2002; 301-54.
3. Murray BE. Vancomycin-resistant enterococcal infections. N Engl J Med 2000; 342: 710-21.
4. Willems RJ, Bonten MJ. Glycopeptide-resistant enterococci: deciphering virulence, resistance and epidemicity. Curr Opin Infect Dis 2007; 20: 384-90.
5. Huycke MM, Sahm DF, Gilmore MS. Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis 1998; 4: 239-49.
6. Huycke MM. Physiology of enterococci. In: Gilmore MS, ed. The Enterococci: Pathogenesis, Molecular Biology, Antibiotic Resistance and Infection Control. Washington, DC, USA: ASM Press, 2002; 133-75.
7. Kearns AM, Freeman R, Lightfoot NF. Nosocomial enterococci: resistance to heat and sodium hypochlorite. J Hosp Infect 1995; 30: 193-9.
8. Boyce JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 2007; 65 Suppl 2: 50-4.
9. Gastmeier P, Schwab F, Barwolff S et al. Correlation between the genetic diversity of nosocomial pathogens and their survival time in intensive care units. J Hosp Infect 2006; 62: 181-6.
10. Drees M, Snydman DR, Schmid CH et al. Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci. Clin Infect Dis 2008; 46: 678-85.
11. Tannock GW, Cook G. Enterococci as members of the intestinal microflora of humans. In: Gilmore MS, ed. The Enterococci: Pathogenesis, Molecular Biology, Antibiotic Resistance and Infection Control. Washington, DC, USA: ASM Press, 2002; 101-32.
12. 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.
13. Paulsen IT, Banerjei L, Myers GS et al. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 2003; 299: 2071-4.
14. Uttley AH, Collins CH, Naidoo J et al. Vancomycin-resistant enterococci. Lancet 1988; i: 57-8.
15. Leclercq R, Derlot E, Duval J et al. Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N Engl J Med 1988; 319: 157-61.
16. Fabbri A, Manno G, Tacchella A et al. Susceptibility of enterococci. I. Inhibitory and bactericidal activity of several chemoantibiotics against Streptococcus faecalis and Streptococcus faecium. Chemioterapia 1986; 5: 302-8.
17. Saribas S, Bagdatli Y. Vancomycin tolerance in enterococci. Chemotherapy 2004; 50: 250-4.
18. Perry JD, Jones AL, Gould FK. Glycopeptide tolerance in bacteria causing endocarditis. J Antimicrob Chemother 1999; 44: 121-4.
19. Sandoe JA, Wysome J, West AP et al. Measurement of ampicillin, vancomycin, linezolid and gentamicin activity against enterococcal biofilms. J Antimicrob Chemother 2006; 57: 767-70.
20. Handwerger S, Tomasz A. Antibiotic tolerance among clinical isolates of bacteria. Rev Infect Dis 1985; 7: 368-86.
21. Hanslik T, Hartig C, Jurand C et al. Clinical significance of tolerant strains of streptococci in adults with infective endocarditis. Clin Microbiol Infect 2003; 9: 852-7.
22. Bizzini A, Entenza JM, Moreillon P. Loss of penicillin tolerance by inactivating the carbon catabolite repression determinant CcpA in Streptococcus gordonii. J Antimicrob Chemother 2007; 59: 607-15.
23. McCullers JA, English BK, Novak R. Isolation and characterization of vancomycin-tolerant Streptococcus pneumoniae from the cerebrospinal fluid of a patient who developed recrudescent meningitis. J Infect Dis 2000; 181: 369-73.
24. Thometz JG, Lamdan R, Kehl KS et al. Microbiological tolerance in orthopaedic infections: delayed response of septic arthritis and osteomyelitis of the hip due to infection with tolerant Staphylococcus aureus. J Pediatr Orthop 1996; 16: 518-21.
25. Safdar A, Rolston KV. Vancomycin tolerance, a potential mechanism for refractory gram-positive bacteremia observational study in patients with cancer. Cancer 2006; 106: 1815-20.
26. McDonald M, Miles H, Hart D et al. Penicillin tolerance in Streptococcus faecalis. Lancet 1980; ii: 321.
27. Cunha BA, Mickail N, Eisenstein L. E. faecalis vancomycinsensitive enterococcal bacteremia unresponsive to a vancomycin tolerant strain successfully treated with high-dose daptomycin. Heart Lung 2007; 36: 456-61.
28. Kohanski MA, Dwyer DJ, Hayete B et al. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 2007; 130: 797-810.
29. Terzaghi BE, Sandine WE. Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol 1975; 29: 807-13.
30. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press, 1989.
31. La Carbona S, Sauvageot N, Giard JC et al. Comparative study of the physiological roles of three peroxidases (NADH peroxidase, alkyl hydroperoxide reductase and thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol Microbiol 2007; 66: 1148-63.
32. Law J, Buist G, Haandrikman A et al. A system to generate chromosomal mutations in Lactococcus lactis which allows fast analysis of targeted genes. J Bacteriol 1995; 177: 7011-8.
33. Woods GL, Washington JA. Antimicrobial susceptibility tests: dilution and disk diffusion methods. In: Murray PR, Baron EJ, Pfaller MA et al., eds. Manual of Clinical Microbiology. Washington, DC, USA: American Society for Microbiology, 1995; 1327-41.
34. Frankenberg L, Brugna M, Hederstedt L. Enterococcus faecalis heme-dependent catalase. J Bacteriol 2002; 184: 6351-6.
35. Verneuil N, Maze 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.
36. Huycke MM, Moore D, Joyce W et al. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol 2001; 42: 729-40.
37. Lefort A, Arthur M, Garry L et al. Bactericidal activity of gentamicin against Enterococcus faecalis in vitro and in vivo. Antimicrob Agents Chemother 2000; 44: 2077-80.
38. Weaver KE, Reddy SG. The recombination deficient Enterococcus faecalis UV202 strain is a recA mutant. Plasmid 2006; 55: 164-8.
39. Sasindran SJ, Saikolappan S, Dhandayuthapani S. Methionine sulfoxide reductases and virulence of bacterial pathogens. Future Microbiol 2007; 2: 619-30.
40. Barnes AI, Herrero IL, Albesa I. New aspect of the synergistic antibacterial action of ampicillin and gentamicin. Int J Antimicrob Agents 2005; 26: 146-51.
41. Huang P, Feng L, Oldham EA et al. Superoxide dismutase as a target for the selective killing of cancer cells. Nature 2000; 407: 390-5.
42. Kachadourian R, Liochev SI, Cabelli DE et al. 2-Methoxyestradiol does not inhibit superoxide dismutase. Arch Biochem Biophys 2001; 392: 349-53.
43. Benov L, Fridovich I. Functional significance of the Cu, ZnSOD in Escherichia coli. Arch Biochem Biophys 1996; 327: 249-53.
44. Takahashi H, Nishina A, Fukumoto RH et al. Selenocarbamates are effective superoxide anion scavengers in vitro. Eur J Pharm Sci 2005; 24: 291-5.
45. 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.
46. Stratton CW. Dead bugs don't mutate: susceptibility issues in the emergence of bacterial resistance. Emerg Infect Dis 2003; 9: 10-6.
47. Albesa I, Becerra MC, Battan PC et al. Oxidative stress involved in the antibacterial action of different antibiotics. Biochem Biophys Res Commun 2004; 317: 605-9.
48. Becerra MC, Albesa I. Oxidative stress induced by ciprofloxacin in Staphylococcus aureus. Biochem Biophys Res Commun 2002; 297: 1003-7.
49. Hassett DJ, Imlay JA. Bactericidal antibiotics and oxidative stress: a radical proposal. ACS Chem Biol 2007; 2: 708-10.
50. Imlay JA. Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 2006; 59: 1073-82.
51. Yagi Y, Clewell DB. Recombination-deficient mutant of Streptococcus faecalis. J Bacteriol 1980; 143: 966-70.
52. Yagi Y, Clewell DB. Amplification of the tetracycline resistance determinant of plasmid pAM alpha 1 in Streptococcus faecalis: dependence on host recombination machinery. J Bacteriol 1980; 143: 1070 2.