Physiological characterisation of the efflux pump system of antibiotic-susceptible and multidrug-resistant Enterobacter aerogenes

International Journal of Antimicrobial Agents

Volumn 36, Issue 4, 2010, Pages 313-318

  Martins, A ^a   Spengler, G ^a   Martins, M ^a   Rodrigues, L ^a   Viveiros, M ^a,b   Davin Regli, A ^b,c   Chevalier, J ^b   Couto, I ^a,d   Pages J M ^b,c   Amaral, L ^a,b  

^a INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^b EUROPEAN COMMISSION   (Belgium)

^c Aix Marseille University   (France)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

Automated ethidium bromide method; Efflux pump overexpression; Enterobacter aerogenes; Modulation by glucose; Modulation by pH; Multidrug resistance

Indexed keywords

ABC TRANSPORTER; CARRIER PROTEIN; CEFEPIME; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; ERYTHROMYCIN; GENTAMICIN; GLUCOSE; IMIPENEM; NALIDIXIC ACID; NORFLOXACIN; OFLOXACIN; PROTEIN ACRAB; SPARFLOXACIN; TETRACYCLINE; TOLC PROTEIN; UNCLASSIFIED DRUG;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; ENTEROBACTER AEROGENES; GENE OVEREXPRESSION; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PH; PHENOTYPE; PRIORITY JOURNAL;

ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROBACTER AEROGENES; ENTEROBACTERIACEAE INFECTIONS; ETHIDIUM; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSE; HUMANS; HYDROGEN-ION CONCENTRATION; MICROBIAL SENSITIVITY TESTS; PROTON-MOTIVE FORCE; UP-REGULATION;

EID: 77955921023     PISSN: 09248579     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijantimicag.2010.06.036     Document Type: Article

References (34)

1. Deal E.N., Micek S.T., Ritchie D.J., Reichley R.M., Dunne W.M., Kollef M.H. Predictors of in-hospital mortality for bloodstream infections caused by Enterobacter species or Citrobacter freundii. Pharmacotherapy 2007, 27:191-199.
2. Goossens H. Antibiotic resistance and policy in Belgium. Verh K Acad Geneeskd Belg 2000, 62:439-469.
3. Giamarellou H. Multidrug resistance in Gram-negative bacteria that produce extended-spectrum β-lactamases (ESBLs). Clin Microbiol Infect 2005, 11:1-16.
4. Davin-Regli A., Bolla J.M., James C.E., Lavigne J.P., Chevalier J., Garnotel E., et al. Membrane permeability and regulation of drug 'influx and efflux' in enterobacterial pathogens. Curr Drug Targets 2008, 9:750-759.
5. Martins A., Iversen C., Rodrigues L., Spengler G., Ramos J., Kern W.V., et al. An AcrAB-mediated multidrug-resistant phenotype is maintained following restoration of wild-type activities by efflux pump genes and their regulators. Int J Antimicrob Agents 2009, 34:602-604.
6. Chevalier J., Mulfinger C., Garnotel E., Nicolas P., Davin-Régli A., Pagès J.M. Identification and evolution of drug efflux pump in clinical Enterobacter aerogenes strains isolated in 1995 and 2003. PLoS One 2008, 3:e3203.
7. Vogelaers D., De Bels D., Forêt F., Cran S., Gilbert E., Schoonheydt K., et al. Patterns of antimicrobial therapy in severe nosocomial infections: empiric choices, proportion of appropriate therapy, and adaptation rates-a multicentre, observational survey in critically ill patients. Int J Antimicrob Agents 2010, 35:375-381.
8. Chang E.P., Chiang D.H., Lin M.L., Chen T.L., Wang F.D., Liu C.Y. Clinical characteristics and predictors of mortality in patients with Enterobacter aerogenes bacteremia. J Microbiol Immunol Infect 2009, 42:329-335.
9. Anderson B., Nicholas S., Sprague B., Campos J., Short B., Singh N. Molecular and descriptive epidemiology of multidrug-resistant Enterobacteriaceae in hospitalized infants. Infect Control Hosp Epidemiol 2008, 29:250-255.
10. Pagès J.M., Amaral L. Mechanisms of drug efflux and strategies to combat them: challenging the efflux pump of Gram-negative bacteria. Biochim Biophys Acta 2009, 1794:826-833.
11. Lomovskaya O., Watkins W.J. Efflux pumps: their role in antibacterial drug discovery. Curr Med Chem 2001, 8:1699-1711.
12. Lomovskaya O., Totrov M. Vacuuming the periplasm. J Bacteriol 2005, 187:1879-1883.
13. Bailey A.M., Paulsen I.T., Piddock L.J. RamA confers multidrug resistance in Salmonella enterica via increased expression of acrB, which is inhibited by chlorpromazine. Antimicrob Agents Chemother 2008, 52:3604-3611.
14. Klitgaard J.K., Skov M.N., Kallipolitis B.H., Kolmos H.J. Reversal of methicillin resistance in Staphylococcus aureus by thioridazine. J Antimicrob Chemother 2008, 62:1215-1221.
15. Viveiros M., Jesus A., Brito M., Leandro C., Martins M., Ordway D., et al. Inducement and reversal of tetracycline resistance in Escherichia coli K-12 and expression of proton gradient-dependent multidrug efflux pump genes. Antimicrob Agents Chemother 2005, 49:3578-3582.
16. Spengler G., Martins A., Rodrigues L., Aagaard L., Martins M., Costa S.S., et al. Characterisation of intrinsic efflux activity of Enterococcus faecalis ATCC29212 by a semi-automated ethidium bromide method. In Vivo 2009, 23:81-87.
17. 1 ATP synthase. Biochemistry 2006, 45:14552-14558.
18. Su C.C., Yu E.W. Ligand-transporter interaction in the AcrB multidrug efflux pump determined by fluorescence polarization assay. FEBS Lett 2007, 81:4972-4976.
19. Martins A., Spengler G., Rodrigues L., Viveiros M., Ramos J., Martins M., et al. pH modulation of efflux pump activity of multi-drug resistant Escherichia coli: protection during its passage and eventual colonization of the colon. PLoS One 2009, 4:e6656.
20. Tran Q.T., Dupont M., Lavigne J.P., Chevalier J., Pagès J.M., Sotto A., et al. Occurrence of efflux mechanism and cephalosporinase variant in a population of Enterobacter aerogenes and Klebsiella pneumoniae isolates producing extended-spectrum β-lactamases. Antimicrob Agents Chemother 2009, 53:1652-1666.
21. Ghisalberti D., Mahamoud A., Chevalier J., Baitiche M., Martino M., Pagès J.M., et al. Chloroquinolines block antibiotic efflux pumps in antibiotic-resistant Enterobacter aerogenes isolates. Int J Antimicrob Agents 2006, 27:565-569.
22. Espinel-Ingroff A., Fothergill A., Ghannoum M., Manavathu E., Ostrosky-Zeichner L., Pfaller M., et al. Quality control and reference guidelines for CLSI broth microdilution susceptibility method (M 38-A document) for amphotericin B, itraconazole, posaconazole, and voriconazole. J Clin Microbiol 2005, 43:5243-5246.
23. Viveiros M., Martins M., Couto I., Rodrigues L., Spengler G., Martins A., et al. New methods for the identification of efflux mediated MDR bacteria, genetic assessment of regulators and efflux pump constituents, characterization of efflux systems and screening for inhibitors of efflux pumps. Curr Drug Targets 2008, 9:760-778.
24. Martins M., Santos B., Martins A., Viveiros M., Couto I., Cruz A., et al. An instrument-free method for the demonstration of efflux pump activity of bacteria. In Vivo 2006, 20:657-664.
25. Viveiros M., Martins A., Paixão L., Rodrigues L., Martins M., Couto I., et al. Demonstration of intrinsic efflux activity of Escherichia coli K-12 AG100 by an automated ethidium bromide method. Int J Antimicrob Agents 2008, 31:458-462.
26. Sharples D., Brown J.R. Correlation of the base specificity of DNA-intercalating ligands with their physico-chemical properties. FEBS Lett 1976, 69:37-40.
27. Ghisalberti D., Masi M., Pagès J.M., Chevalier J. Chloramphenicol and expression of multidrug efflux pump in Enterobacter aerogenes. Biochem Biophys Res Commun 2005, 328:1113-1118.
28. Chevalier J., Mahamoud A., Baitiche M., Adam A., Viveiros M., Smarandache A., et al. Quinazoline derivatives are efficient chemosensitizers of antibiotic activity in Enterobacter aerogenes, Klebsiella pneumoniae and Pseudomonas aeruginosa resistant strains. Int J Antimicrob Agents 2010, 36:164-168.
29. Viveiros M., Portugal I., Bettencourt R., Victor T.C., Jordaan A.M., Leandro C., et al. Isoniazid-induced transient high-level resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 2002, 46:2804-2810.
30. Mulkidjanian A.Y., Heberle J., Cherepanov D.A. Protons @ interfaces: implications for biological energy conversion. Biochim Biophys Acta 2006, 1757:913-930.
31. Kadlec K., Kehrenberg C., Schwarz S. Efflux-mediated resistance to florfenicol and/or chloramphenicol in Bordetella bronchiseptica: identification of a novel chloramphenicol exporter. J Antimicrob Chemother 2007, 59:191-196.
32. Begic S., Worobec E.A. Fluoroquinolone resistance of Serratia marcescens: sucrose, salicylate, temperature, and pH induction of phenotypic resistance. Can J Microbiol 2007, 53:1239-1245.
33. Lomovskaya O., Zgurskaya H.I., Totrov M., Watkins W.J. Waltzing transporters and 'the dance macabre' between humans and bacteria. Nat Rev Drug Discov 2007, 6:56-65.
34. Tal N., Schuldiner S. A coordinated network of transporters with overlapping specificities provides a robust survival strategy. Proc Natl Acad Sci U S A 2009, 106:9051-9056.