The Efflux Inhibitor Phenylalanine-Arginine Beta-Naphthylamide (PAβN) Permeabilizes the Outer Membrane of Gram-Negative Bacteria

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Lamers, Ryan P ^a   Cavallari, Joseph F ^a   Burrows, Lori L ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ADJUVANT; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE AMPC; CEFOTAXIME; CEFTAZIDIME; CIPROFLOXACIN; PHENYLALANINE ARGININE BETA NAPHTHYLAMIDE; PIPERACILLIN; UNCLASSIFIED DRUG; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; COLONY FORMING UNIT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; GROWTH INHIBITION; MEMBRANE PERMEABILITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PLASMID; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA;

ANILINO NAPHTHALENESULFONATES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAMASES; BETA-LACTAMS; CELL MEMBRANE PERMEABILITY; CULTURE MEDIA; DETERGENTS; DIPEPTIDES; DRUG RESISTANCE, BACTERIAL; GRAM-NEGATIVE BACTERIA; MAGNESIUM; MICROBIAL SENSITIVITY TESTS; PERIPLASM; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84875478948     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060666     Document Type: Article

References (39)

1. Zavascki AP, Goldani LZ, Li J, Nation RL, (2007) Polymyxin B for the treatment of multidrug-resistant pathogens: a critical review. The Journal of Antimicrobial Chemotherapy 60: 1206-1215.
2. Lister PD, Wolter DJ, Hanson ND, (2009) Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clinical Microbiology Reviews 22: 582-610.
3. Mark BL, Vocadlo DJ, Oliver A, (2011) Providing beta-lactams a helping hand: targeting the AmpC beta-lactamase induction pathway. Future Microbiology 6: 1415-1427.
4. Nicola G, Tomberg J, Pratt RF, Nicholas RA, Davies C, (2010) Crystal structures of covalent complexes of beta-lactam antibiotics with Escherichia coli penicillin-binding protein 5: toward an understanding of antibiotic specificity. Biochemistry 49: 8094-8104.
5. Beadle BM, Nicholas RA, Shoichet BK, (2001) Interaction energies between beta-lactam antibiotics and E. coli penicillin-binding protein 5 by reversible thermal denaturation. Protein Science 10: 1254-1259.
6. Jacobs C, Huang LJ, Bartowsky E, Normark S, Park JT, (1994) Bacterial cell wall recycling provides cytosolic muropeptides as effectors for beta-lactamase induction. The EMBO Journal 13: 4684-4694.
7. Moya B, Dotsch A, Juan C, Blazquez J, Zamorano L, et al. (2009) Beta-lactam resistance response triggered by inactivation of a nonessential penicillin-binding protein. PLoS Pathogens 5: e1000353.
8. Piddock LJ, (2006) Multidrug-resistance efflux pumps- not just for resistance. Nature Reviews Microbiology 4: 629-636.
9. Askoura M, Mottawea W, Abujamel T, Taher I, (2011) Efflux pump inhibitors (EPIs) as new antimicrobial agents against Pseudomonas aeruginosa. The Libyan Journal of Medicine 6doi:10.3402/ljm.v6i0.5870.
10. Piddock LJ, (2006) Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clinical Microbiology Reviews 19: 382-402.
11. Webber MA, Piddock LJ, (2003) The importance of efflux pumps in bacterial antibiotic resistance. The Journal of Antimicrobial Chemotherapy 51: 9-11.
12. Li XZ, Nikaido H, Poole K, (1995) Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 39: 1948-1953.
13. Li XZ, Zhang L, Poole K, (2000) Interplay between the MexA-MexB-OprM multidrug efflux system and the outer membrane barrier in the multiple antibiotic resistance of Pseudomonas aeruginosa. The Journal of Antimicrobial Chemotherapy 45: 433-436.
14. Srikumar R, Tsang E, Poole K, (1999) Contribution of the MexAB-OprM multidrug efflux system to the beta-lactam resistance of penicillin-binding protein and beta-lactamase-derepressed mutants of Pseudomonas aeruginosa. The Journal of Antimicrobial Chemotherapy 44: 537-540.
15. Lomovskaya O, Warren MS, Lee A, Galazzo J, Fronko R, et al. (2001) Identification and characterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrobial Agents and Chemotherapy 45: 105-116.
16. Renau TE, Leger R, Flamme EM, Sangalang J, She MW, et al. (1999) Inhibitors of efflux pumps in Pseudomonas aeruginosa potentiate the activity of the fluoroquinolone antibacterial levofloxacin. Journal of Medicinal Chemistry 42: 4928-4931.
17. Matsumoto Y, Hayama K, Sakakihara S, Nishino K, Noji H, et al. (2011) Evaluation of multidrug efflux pump inhibitors by a new method using microfluidic channels. PLoS ONE 6: e18547.
18. Zechini B, Versace I, (2009) Inhibitors of multidrug resistant efflux systems in bacteria. Recent Patents on Anti-infective Drug Discovery 4: 37-50.
19. Schweizer HP, (2012) Understanding efflux in Gram-negative bacteria: opportunities for drug discovery. Expert Opinion on Drug Discovery 7: 633-642.
20. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP, (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
21. Balemans W, Vranckx L, Lounis N, Pop O, Guillemont J, et al. (2012) Novel antibiotics targeting respiratory ATP synthesis in Gram-positive pathogenic bacteria. Antimicrobial Agents and Chemotherapy 56: 4131-4139.
22. Drusano GL, Bonomo RA, Bahniuk N, Bulitta JB, Vanscoy B, et al. (2012) Resistance emergence mechanism and mechanism of resistance suppression by tobramycin for cefepime for Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 56: 231-242.
23. Loh B, Grant C, Hancock RE, (1984) Use of the fluorescent probe 1-N-phenylnaphthylamine to study the interactions of aminoglycoside antibiotics with the outer membrane of Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 26: 546-551.
24. Poole K, (2005) Efflux-mediated antimicrobial resistance. The Journal of Antimicrobial Chemotherapy 56: 20-51.
25. Kus JV, Gebremedhin A, Dang V, Tran SL, Serbanescu A, et al. (2011) Bile salts induce resistance to polymyxin in enterohemorrhagic Escherichia coli O157:H7. Journal of Bacteriology 193: 4509-4515.
26. Thanassi DG, Cheng LW, Nikaido H, (1997) Active efflux of bile salts by Escherichia coli. Journal of Bacteriology 179: 2512-2518.
27. Nikaido H, (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews 67: 593-656.
28. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
29. Mulet X, Moya B, Juan C, Macia MD, Perez JL, et al. (2011) Antagonistic interactions of Pseudomonas aeruginosa antibiotic resistance mechanisms in planktonic but not biofilm growth. Antimicrobial Agents and Chemotherapy 55: 4560-4568.
30. Stickland HG, Davenport PW, Lilley KS, Griffin JL, Welch M, (2010) Mutation of nfxB causes global changes in the physiology and metabolism of Pseudomonas aeruginosa. Journal of Proteome Research 9: 2957-2967.
31. Poole K, (2001) Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. Journal of Molecular Microbiology and Biotechnology 3: 255-264.
32. Zhang L, Dhillon P, Yan H, Farmer S, Hancock RE, (2000) Interactions of bacterial cationic peptide antibiotics with outer and cytoplasmic membranes of Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy 44: 3317-3321.
33. Suzuki H, Wang ZY, Yamakoshi M, Kobayashi M, Nozawa T, (2003) Probing the transmembrane potential of bacterial cells by voltage-sensitive dyes. Analytical Sciences 19: 1239-1242.
34. Lomovskaya O, Watkins W, (2001) Inhibition of efflux pumps as a novel approach to combat drug resistance in bacteria. Journal of Molecular Microbiology and Biotechnology 3: 225-236.
35. Mahamoud A, Chevalier J, Alibert-Franco S, Kern WV, Pages JM, (2007) Antibiotic efflux pumps in Gram-negative bacteria: the inhibitor response strategy. The Journal of Antimicrobial Chemotherapy 59: 1223-1229.
36. Lomovskaya O, Bostian KA, (2006) Practical applications and feasibility of efflux pump inhibitors in the clinic--a vision for applied use. Biochemical Pharmacology 71: 910-918.
37. Yu EW, Aires JR, McDermott G, Nikaido H, (2005) A periplasmic drug-binding site of the AcrB multidrug efflux pump: a crystallographic and site-directed mutagenesis study. Journal of Bacteriology 187: 6804-6815.
38. Pages JM, Masi M, Barbe J, (2005) Inhibitors of efflux pumps in Gram-negative bacteria. Trends in Molecular Medicine 11: 382-389.
39. Nikaido H, (1998) The role of outer membrane and efflux pumps in the resistance of gram-negative bacteria. Can we improve drug access? Drug Resistance Updates 1: 93-98.