Evaluation of forty new phenothiazine derivatives for activity against intrinsic efflux pump systems of reference Escherichia coli, Salmonella enteritidis, Enterococcus faecalis and Staphylococcus aureus strains

In Vivo

Volumn 25, Issue 5, 2011, Pages 719-724

  Takács, Daniella ^a   Cerca, Pedro ^b   Martins, Ana ^c   Riedl, Zsuzsanna ^a   Hajós, György ^a   Molnár, Joseph ^d,e   Viveiros, Miguel ^b,e   Couto, Isabel ^b,f   Amaral, Leonard ^b,e  

^a CHEMICAL RESEARCH CENTER   (Hungary)

^b INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^c UNIVERSITY OF SZEGED   (Hungary)

^d UNIVERSITY OF SZEGED   (Hungary)

^e Faculty of Sciences and Technology ^*  (Portugal)

^f UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

Enterococcus faecalis; Escherichia coli; Inhibition of efflux pumps; Multidrug resistance; Over expressed efflux pumps; Pathogenic bacteria; Phenothiazine derivatives; Reduction of resistance; Salmonella enteritidis; Staphylococcus aureus

Indexed keywords

CHLORPROMAZINE; METHYLENE BLUE; PHENOTHIAZINE DERIVATIVE; PROMETHAZINE; THIORIDAZINE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL STRAIN; DRUG EFFECT; DRUG STRUCTURE; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; SALMONELLA ENTERITIDIS; STAPHYLOCOCCUS AUREUS;

EID: 79960639569     PISSN: 0258851X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (31)

1. Pagès JM and Amaral L: Mechanisms of drug efflux and strategies to combat them: challenging the efflux pump of Gram-negative bacteria. Biochim Biophys Acta 1794: 826-833, 2009.
2. Viveiros M, Jesus A, Brito M, Leandro C, Martins M, Ordway D, Molnar AM, Molnar J and Amaral L: Inducement and reversal of tetracycline resistance in Escherichia coli K-12 and expression of proton gradient-dependent multidrug efflux pump genes. Antimicrob Agents Chemother 49: 3578-3582, 2005. (Pubitemid 41060625)
3. Martins A, Iversen C, Rodrigues L, Spengler G, Ramos J, Kern WV, Couto I, Viveiros M, Fanning S, Pages JM and Amaral L: 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 34: 602-604, 2009.
4. Martins A, Spengler G, Rodrigues L, Viveiros M, Ramos J, Martins M, Couto I, Fanning S, Pagès JM, Bolla JM, Molnar J and Amaral L: pH Modulation of efflux pump activity of multi-drug resistant Escherichia coli: protection during its passage and eventual colonization of the colon. PLoS One 4(8): e6656, 2009.
5. Chevalier J, Mahamoud A, Baitiche M, Adam E, Viveiros M, Smarandache A, Militaru A, Pascu ML, Amaral L and Pagès JM: Quinazoline derivatives are efficient chemosensitizers of antibiotic activity in Enterobacter aerogenes, Klebsiella pneumoniae and Pseudomonas aeruginosa resistant strains. Int J. Antimicrob Agents 36: 164-168, 2010.
6. Martins A, Couto I, Aagaard L, Martins M, Viveiros M, Kristiansen JE and Amaral L: Prolonged exposure of methicillin-resistant Staphylococcus aureus (MRSA) COL strain to increasing concentrations of oxacillin results in a multidrug-resistant phenotype. Int J Antimicrob Agents 29: 302-305, 2007. (Pubitemid 46240753)
7. Spengler G, Martins A, Schelz Z, Rodrigues L, Aagaard L, Martins M, Costa SS, Couto I, Viveiros M, Fanning S, Kristiansen JE, Molnar J and Amaral L: Characterization of intrinsic efflux activity of Enterococcus faecalis ATCC29212 by a semi-automated ethidium bromide method. In Vivo 23: 81-87, 2009.
8. Viveiros M, Dupont M, Rodrigues L, Couto I, Davin-Regli A, Martins M, Pagès JM and Amaral L: Antibiotic stress, genetic response and altered permeability of Escherichia coli. PLoS One 2: e365, 2007.
9. Viveiros M, Rodrigues L, Martins M, Couto I, Spengler G, Martins A and Amaral L: Evaluation of efflux activity of bacteria by a semi-automated fluorometric system. Methods Mol Biol 642: 59-72, 2010.
10. Paixão L, Rodrigues L, Couto I, Martins M, Fernandes P, de Carvalho CC, Monteiro GA, Sansonetty F, Amaral L and Viveiros M: Fluorometric determination of ethidium bromide efflux kinetics in Escherichia coli. J Biol Eng 3: 3-18, 2009.
11. Martins A, Machado L, Costa S, Cerca P, Spengler G, Viveiros M and Amaral L: Role of calcium in efflux system of E. coli. Int J Antimicrob Agents 37: 410-414, 2011.
12. Martins A, Vasas A, Viveiros M, Molnar J, Hohmann J and Amaral L: Antibacterial properties of compounds isolated from Carpobrotus edulis. Int J Antimicrob Agents 37: 410-414, 2011.
13. Martins A, Spengler G, Martin M, Rodrigues L, Viveiros M, Davin-Regli A, Chevalier J, Couto I, Pagès JM and Amaral L: Physiological characterization of the efflux pump system of antibiotic susceptible and multi-drug resistant Enterobacter aerogenes. Int J Antimicrob Agents 36: 313-318, 2010.
14. Amaral L, Pages JM and Fanning S: RND efflux pumps of Gram-negative bacteria. Advances In Enzymology 77: 61-108, 2011.
15. Nikaido H and Zgurskaya H I: AcrAB and related multidrug efflux pumps of Escherichia coli. J Mol Microbiol Biotechnol 3: 215-218, 2001. (Pubitemid 32257906)
16. Okusu H, Ma D and Nikaido H: AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic- resistance (Mar) mutants. J Bacteriol 178: 306-308, 1996.
17. Costa SS, Falcão C, Viveiros M, Machado D, Martins M, Melo-Cristino J, Amaral L, and Couto I: Exploring the contribution of efflux on the resistance to fluoroquinolones in clinical isolates of Staphylococcus aureus. Submitted to BMC Microbiol.
18. Costa SS, Ntokou E, Martins A, Viveiros M, Pournaras S, Couto I and Amaral L: Identification of the plasmid-encoded qacA efflux pump gene in meticillin-resistant Staphylococcus aureus (MRSA) strain HPV107, a representative of the MRSA Iberian clone. Int J Antimicrob Agents 36: 557-561, 2010.
19. O'Regan E, Quinn T, Pagès JM, McCusker M, Piddock L and Fanning S: Multiple regulatory pathways associated with high-level ciprofloxacin and multidrug resistance in Salmonella enterica serovar Enteritidis: involvement of ramA and other global regulators. Antimicrob Agents Chemother 53: 1080-1087, 2009.
20. Amaral L, Viveiros M, Fanning S, Pages JM, Couto I, Spengler G, Rodrigues L and Martins A: Genetic regulation, physiology, assessment and inhibition of efflux pumps responsible for multi-drug resistant phenotypes of bacterial pathogens. In: Antibiotic Resistance: Causes and Risk Factors, Mechanisms and Alternatives. Bonilla AR and Muniz KP (eds.); New York, Nova Science Publishers, Inc., pp. 313-332, 2009.
21. Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Informational Supplement. CLSI document 27(1): M100-S17, 2007.
22. Kristiansen JE, Thomsen VF, Martins A, Viveiros M and Amaral L: Non-antibiotics reverse resistance of bacteria to antibiotics. In Vivo 5: 751-754, 2010.
23. Hendricks O, Molnar A, Butterworth TS, Butaye P, Kolmos HJ, Christensen JB and Kristiansen JE: In vitro activity of phenothiazine derivatives in Enterococcus faecalis and Enterococcus faecium. Basic Clin Pharmacol Toxicol 96: 33-36, 2005.
24. Kristiansen JE, Hendricks O, Delvin T, Butterworth TS, Aagaard L, Christensen JB, Flores VC and Keyzer H: Reversal of resistance in microorganisms by help of non-antibiotics. J Antimicrob Chemother 59: 1271-1279, 2007. (Pubitemid 47073346)
25. Amaral L, Cerca P, Spengler G, Machado L, Couto I, Viveiros M, Fanning S and Pagès JM: Ethidium bromide efflux by Salmonella: Modulation by metabolic energy, pH, ions and phenothiazines. Int J Antimicrob Agents 2011; In Press.
26. Pagès JM, Amaral L and Fanning S: An original deal for new molecule: Reversal of efflux pump activity, a rational strategy to combat Gram-negative resistant bacteria. Curr Med Chem 2011; In Press.
27. Cadilla A, David MZ, Daum RS and Boyle-Vavra S: Association of high-level mupirocin resistance and multidrug-resistant methicillin-resistant Staphylococcus aureus at an academic center in the midwestem United States. J Clin Microbiol 49: 95-100, 2011.
28. Turnidge JD and Bell JM: Methicillin-resistant Staphylococcus aureus evolution in Australia over 35 years. Microb Drug Resist 6: 223-229, 2000.
29. Cassone M, Campanile F, Pantosti A, Venditti M and Stefani S: Identification of a variant "Rome clone" of methicillin-resistant Staphylococcus aureus with decreased susceptibility to vancomycin, responsible for an outbreak in an intensive care unit. Microb Drug Resist 10: 43-49, 2004.
30. Bailey AM, Paulsen IT and Piddock LJ: RamA confers multidrug resistance in Salmonella enterica via increased expression of acrB, which is inhibited by chlorpromazine. Antimicrob Agents Chemother 52: 3604-3611, 2008.
31. Amaral L, Kristiansen JE, Thomsen VF and Markowich B: The effect of chlorpromazine on the outer cell wall constituents of Salmonella typhimurium ensuring resistance to the drug. Int J Antimicrob Agents 14: 225-229, 2000. (Pubitemid 30201548)