Resistance-Nodulation-Division multidrug efflux pumps in Gram-negative bacteria: Role in virulence

Antibiotics

Volumn 2, Issue 1, 2013, Pages 163-181

  Fernando, Dinesh M ^a   Kumar, Ayush ^a  

^a UNIVERSITY OF ONTARIO INSTITUTE OF TECHNOLOGY   (Canada)

Author keywords

Biofilm; Gram negative bacteria; Host colonization; Multidrug efflux systems; Oxidative stress

Indexed keywords

ACRAB PUMP; AMINOGLYCOSIDE; BACTERIAL PROTEIN; CHLORAMPHENICOL; CIPROFLOXACIN; CMEABC PUMP; ETHIDIUM BROMIDE; MACROLIDE; MEXAB-OPRM PUMP; MEXCD-OPRJ PUMP; MEXEF-OPRN PUMP; MEXXY PUMP; MTRCDE PUMP; MUXBC-OPMB PUMP; NITROFURANTOIN; NOVOBIOCIN; OUTER MEMBRANE PROTEIN; POLYMYXIN B; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; RESISTANCE NODULATION DIVISION EFFLUX PUMP PROTEIN; RIFAMPICIN; TETRACYCLINE; TRICLOSAN; TRIMETHOPRIM; UNCLASSIFIED DRUG; UNINDEXED DRUG; VEXAB PUMP; VEXCD PUMP; VEXIJK PUMP;

BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BIOFILM; GENE MUTATION; GENE OVEREXPRESSION; GRAM NEGATIVE BACTERIUM; HUMAN; MULTIDRUG RESISTANCE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REVIEW; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 85011883284     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics2010163     Document Type: Review

References (98)

1. Jones, D. S.; Podolsky, S. H.; Greene, J. A. The burden of disease and the changing task of medicine. N. Engl. J. Med. 2012, 366, 2333-2338.
2. Finland, M. Emergence of Antibiotic-Resistant Bacteria. N. Engl. J. Med. 1955, 253, 1019-1028.
3. Fauci, A. S. Infectious Diseases: Considerations for the 21st Century. Clin. Infect. Dis. 2001, 32, 675-685.
4. Poole, K. Efflux-mediated multiresistance in Gram-negative bacteria. Clin. Microbiol. Infect. 2004, 10, 12-26.
5. Nikaido, H.; Pages, J. M. Broad-specificity efflux pumps and their role in multidrug resistance of Gram-negative bacteria. FEMS Microbiol. Rev. 2012, 36, 340-363.
6. McMurry, L.; Petrucci, R. E., Jr.; Levy, S. B. Active efflux of tetracycline encoded by four genetically different tetracycline resistance determinants in Escherichia coli. Proc. Natl. Acad. Sci. USA 1980, 77, 3974-3977.
7. Demerec, M. Patterns of bacterial resistance to penicillin, aureomycin, and streptomycin. J. Clin. Invest. 1949, 28, 891-893.
8. Schmalstieg, A. M.; Srivastava, S.; Belkaya, S.; Deshpande, D.; Meek, C.; Leff, R.; van Oers, N. S. C.; Gumbo, T. The antibiotic resistance arrow of time: Efflux pump induction is a general first step in the evolution of mycobacterial drug resistance. Antimicrob. Agents Chemother. 2012, 56, 4806-4815.
9. Paulsen, I. T. Multidrug efflux pumps and resistance: Regulation and evolution. Curr. Opin. Microbiol. 2003, 6, 446-451.
10. Ma, D.; Cook, D. N.; Alberti, M.; Pon, N. G.; Nikaido, H.; Hearst, J. E. Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J. Bacteriol. 1993, 175, 6299-6313.
11. Poole, K.; Krebes, K.; McNally, C.; Neshat, S. Multiple antibiotic resistance in Pseudomonas aeruginosa: Evidence for involvement of an efflux operon. J. Bacteriol. 1993, 175, 7363-7372.
12. Akama, H.; Kanemaki, M.; Yoshimura, M.; Tsukihara, T.; Kashiwagi, T.; Yoneyama, H.; Narita, S.; Nakagawa, A.; Nakae, T. Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa: Dual modes of membrane anchoring and occluded cavity end. J. Biol. Chem. 2004, 279, 52816-52819.
13. Akama, H.; Matsuura, T.; Kashiwagi, S.; Yoneyama, H.; Narita, S.-I.; Tsukihara, T.; Nakagawa, A.; Nakae, T. Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J. Biol. Chem. 2004, 279, 25939-25942.
14. Koronakis, V.; Sharff, A.; Koronakis, E.; Luisi, B.; Hughes, C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 2000, 405, 914-919.
15. Murakami, S.; Nakashima, R.; Yamashita, E.; Yamaguchi, A. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 2002, 419, 587-593.
16. Li, X.-Z.; Nikaido, H. Efflux-mediated drug resistance in bacteria: An update. Drugs 2009, 69, 1555-1623.
17. Zgurskaya, H. I. Multicomponent drug efflux complexes: Architecture and mechanism of assembly. Future Microbiol. 2009, 4, 919-932.
18. Tseng, T. T.; Gratwick, K. S.; Kollman, J.; Park, D.; Nies, D. H.; Goffeau, A.; Saier, M. H., Jr. The RND permease superfamily: An ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol. 1999, 1, 107-125.
19. Shen, Z.; Pu, X.-Y.; Zhang, Q. Salicylate functions as an efflux pump inducer and promotes the emergence of fluoroquinolone-resistant mutants in Campylobacter jejuni. Appl. Environ. Microbiol. 2011, 77, 7128-7133.
20. Saito, K.; Yoneyama, H.; Nakae, T. nalB-type mutations causing the overexpression of the MexAB-OprM efflux pump are located in the mexR gene of the Pseudomonas aeruginosa chromosome. FEMS Microbiol. Lett. 1999, 179, 67-72.
21. Wang, H.; Dzink-Fox, J. L.; Chen, M.; Levy, S. B. Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: Role of acrR mutations. Antimicrob. Agents Chemother. 2001, 45, 1515-1521.
22. Rosenberg, E. Y.; Bertenthal, D.; Nilles, M. L.; Bertrand, K. P.; Nikaido, H. Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol. Microbiol. 2003, 48, 1609-1619.
23. Chuanchuen, R.; Beinlich, K.; Hoang, T. T.; Becher, A.; Karkhoff-Schweizer, R. R.; Schweizer, H. P. Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: Exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob. Agents Chemother. 2001, 45, 428-432.
24. Camarena, L.; Bruno, V.; Euskirchen, G.; Poggio, S.; Snyder, M. Molecular mechanisms of ethanol-induced pathogenesis revealed by RNA-sequencing. PLoS Pathog. 2010, 6, e1000834.
25. Ma, D.; Alberti, M.; Lynch, C.; Nikaido, H.; Hearst, J. E. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 1996, 19, 101-112.
26. Adebusuyi, A.; Foght, J. An alternative physiological role for the EmhABC efflux pump in Pseudomonas fluorescens cLP6a. BMC Microbiol. 2011, 11, e252.
27. Hartog, E.; Ben-Shalom, L.; Shachar, D.; Matthews, K. R.; Yaron, S. Regulation of marA, soxS, rob, acrAB and micF in Salmonella enterica serovar Typhimurium. Microbiol. Immunol. 2008, 52, 565-574.
28. Ma, D.; Cook, D. N.; Alberti, M.; Pon, N. G.; Nikaido, H.; Hearst, J. E. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol. Microbiol. 1995, 16, 45-55.
29. Li, X.; Zolli-Juran, M.; Cechetto, J. D.; Daigle, D. M.; Wright, G. D.; Brown, E. D. Multicopy suppressors for novel antibacterial compounds reveal targets and drug efflux susceptibility. Chem. Biol. 2004, 11, 1423-1430.
30. Caughlan, R. E.; Jones, A. K.; DeLucia, A. M.; Woods, A. L.; Xie, L.; Ma, B.; Barnes, S. W.; Walker, J. R.; Sprague, E. R.; Yang, X.; et al. Mechanisms decreasing in vitro susceptibility to the LpxC inhibitor CHIR-090 in the Gram-negative pathogen Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2012, 56, 17-27.
31. Join-Lambert, O. F.; Michea-Hamzehpour, M.; Koehler, T.; Chau, F.; Faurisson, F.; Dautrey, S.; Vissuzaine, C.; Carbon, C.; Pechere, J.-C. Differential selection of multidrug efflux mutants by trovafloxacin and ciprofloxacin in an experimental model of Pseudomonas aeruginosa acute pneumonia in rats. Antimicrob. Agents Chemother. 2001, 45, 571-576.
32. Hirakata, Y.; Srikumar, R.; Poole, K.; Gotoh, N.; Suematsu, T.; Kohno, S.; Kamihira, S.; Hancock, R. E.; Speert, D. P. Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J. Exp. Med. 2002, 196, 109-118.
33. Hirakata, Y.; Kondo, A.; Hoshino, K.; Yano, H.; Arai, K.; Hirotani, A.; Kunishima, H.; Yamamoto, N.; Hatta, M.; Kitagawa, M.; et al. Efflux pump inhibitors reduce the invasiveness of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 2009, 34, 343-346.
34. Mima, T.; Kohira, N.; Li, Y.; Sekiya, H.; Ogawa, W.; Kuroda, T.; Tsuchiya, T. Gene cloning and characteristics of the RND-type multidrug efflux pump MuxABC-OpmB possessing two RND components in Pseudomonas aeruginosa. Microbiology 2009, 155, 3509-3517.
35. Yang, L.; Chen, L.; Shen, L.; Surette, M.; Duan, K. Inactivation of MuxABC-OpmB transporter system in Pseudomonas aeruginosa leads to increased ampicillin and carbenicillin resistance and decreased virulence. J. Microbiol. 2011, 49, 107-114.
36. Buroni, S.; Pasca, M. R.; Flannagan, R. S.; Bazzini, S.; Milano, A.; Bertani, I.; Venturi, V.; Valvano, M. A.; Riccardi, G. Assessment of three Resistance-Nodulation-Cell Division drug efflux transporters of Burkholderia cenocepacia in intrinsic antibiotic resistance. BMC Microbiol. 2009, 9, e200.
37. Bazzini, S.; Udine, C.; Sass, A.; Pasca, M. R.; Longo, F.; Emiliani, G.; Fondi, M.; Perrin, E.; Decorosi, F.; Viti, C.; et al. Deciphering the role of RND efflux transporters in Burkholderia cenocepacia. PLoS One 2011, 6, e18902.
38. Hwang, S.; Zhang, Q.; Ryu, S.; Jeon, B. Transcriptional regulation of the CmeABC multidrug efflux pump and the KatA catalase by CosR in Campylobacter jejuni. J. Bacteriol. 2012, 194, 6883-6891.
39. Lin, J.; Michel, L. O.; Zhang, Q. CmeABC functions as a multidrug efflux system in Campylobacter jejuni. Antimicrob. Agents Chemother. 2002, 46, 2124-2131.
40. Burse, A.; Weingart, H.; Ullrich, M. S., The Phytoalexin-inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora. Mol. Plant Microbe Interact. 2004, 17, 43-54.
41. Kohanski, M. A.; DePristo, M. A.; Collins, J. J. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 2010, 37, 311-320.
42. White, D. G.; Goldman, J. D.; Demple, B.; Levy, S. B. Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli. J. Bacteriol. 1997, 179, 6122-6126.
43. Hagman, K. E.; Pan, W.; Spratt, B. G.; Balthazar, J. T.; Judd, R. C.; Shafer, W. M. Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 1995, 141, 611-622.
44. Jerse, A. E.; Sharma, N. D.; Simms, A. N.; Crow, E. T.; Snyder, L. A.; Shafer, W. M. A gonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect. Immun. 2003, 71, 5576-5582.
45. Rouquette, C.; Harmon, J. B.; Shafer, W. M. Induction of the mtrCDE-encoded efflux pump system of Neisseria gonorrhoeae requires MtrA, an AraC-like protein. Mol. Microbiol. 1999, 33, 651-658.
46. Warner, D. M.; Folster, J. P.; Shafer, W. M.; Jerse, A. E. Regulation of the MtrC-MtrD-MtrE efflux-pump system modulates the in vivo fitness of Neisseria gonorrhoeae. J. Infect. Dis. 2007, 196, 1804-1812.
47. Evans, K.; Passador, L.; Srikumar, R.; Tsang, E.; Nezezon, J.; Poole, K. Influence of the MexAB-OprM multidrug efflux system on quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 1998, 180, 5443-5447.
48. Li, X. Z.; Nikaido, H.; Poole, K. Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1995, 39, 1948-1953.
49. Poole, K.; Gotoh, N.; Tsujimoto, H.; Zhao, Q.; Wada, A.; Yamasaki, T.; Neshat, S.; Yamagishi, J.-I.; Li, X.-Z.; Nishino, T. Overexpression of the mexC-mexD-oprJ efflux operon in nfxB-type multidrug-resistant strains of Pseudomonas aeruginosa. Mol. Microbiol. 1996, 21, 713-725.
50. Fetar, H.; Gilmour, C.; Klinoski, R.; Daigle, D. M.; Dean, C. R.; Poole, K. mexEF-oprN multidrug efflux operon of Pseudomonas aeruginosa: Regulation by the MexT activator in response to nitrosative stress and chloramphenicol. Antimicrob. Agents Chemother. 2011, 55, 508-514.
51. Kohler, T.; Michea-Hamzehpour, M.; Henze, U.; Gotoh, N.; Curty, L. K.; Pechere, J. C. Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol. Microbiol. 1997, 23, 345-354.
52. Kohler, T.; van Delden, C.; Curty, L. K.; Hamzehpour, M. M.; Pechere, J.-C. Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa. J. Bacteriol. 2001, 183, 5213-5222.
53. Fraud, S.; Poole, K. Oxidative stress induction of the MexXY multidrug efflux genes and promotion of aminoglycoside resistance development in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2011, 55, 1068-1074.
54. Hocquet, D.; Vogne, C.; El Garch, F.; Vejux, A.; Gotoh, N.; Lee, A.; Lomovskaya, O.; Plesiat, P. MexXY-OprM efflux pump is necessary for a adaptive resistance of Pseudomonas aeruginosa to aminoglycosides. Antimicrob. Agents Chemother. 2003, 47, 1371-1375.
55. Vogne, C.; Aires, J. R.; Bailly, C.; Hocquet, D.; Plesiat, P. Role of the multidrug efflux system MexXY in the emergence of moderate resistance to aminoglycosides among Pseudomonas aeruginosa isolates from patients with cystic fibrosis. Antimicrob. Agents Chemother. 2004, 48, 1676-1680.
56. Stoitsova, S. O.; Braun, Y.; Ullrich, M. S.; Weingart, H. Characterization of the RND-Type multidrug efflux pump MexAB-OprM of the plant pathogen Pseudomonas syringae. Appl. Environ. Microbiol. 2008, 74, 3387-3393.
57. Baucheron, S.; Mouline, C.; Praud, K.; Chaslus-Dancla, E.; Cloeckaert, A. TolC but not AcrB is essential for multidrug-resistant Salmonella enterica serotype Typhimurium colonization of chicks. J. Antimicrob. Chemother. 2005, 55, 707-712.
58. Kehrenberg, C.; Cloeckaert, A.; Klein, G.; Schwarz, S. Decreased fluoroquinolone susceptibility in mutants of Salmonella serovars other than Typhimurium: Detection of novel mutations involved in modulated expression of ramA and soxS. J. Antimicrob. Chemother. 2009, 64, 1175-1180.
59. Lacroix, F. J.; Cloeckaert, A.; Grepinet, O.; Pinault, C.; Popoff, M. Y.; Waxin, H.; Pardon, P. Salmonella Typhimurium acrB-like gene: Identification and role in resistance to biliary salts and detergents and in murine infection. FEMS Microbiol. Lett. 1996, 135, 161-167.
60. Nikaido, H.; Basina, M.; Nguyen, V.; Rosenberg, E. Y. Multidrug efflux pump AcrAB of Salmonella typhimurium excretes only those beta-lactam antibiotics containing lipophilic side chains. J. Bacteriol. 1998, 180, 4686-4692.
61. Piddock, L. J.; White, D. G.; Gensberg, K.; Pumbwe, L.; Griggs, D. J. Evidence for an efflux pump mediating multiple antibiotic resistance in Salmonella enterica serovar Typhimurium. Antimicrob. Agents Chemother. 2000, 44, 3118-3121.
62. Bina, X. R.; Provenzano, D.; Nguyen, N.; Bina, J. E. Vibrio cholerae RND family efflux systems are required for antimicrobial resistance, optimal virulence factor production, and colonization of the infant mouse small intestine. Infect. Immun. 2008, 76, 3595-3605.
63. Taylor, D. L.; Bina, X. R.; Bina, J. E. Vibrio cholerae vexH encodes a multiple drug efflux pump that contributes to the production of cholera toxin and the toxin co-regulated pilus. PLoS One 2012, 7, e38208.
64. Linares, J. F.; López, J. A.; Camafeita, E.; Albar, J. P.; Rojo, F.; Martínez, J. L. Overexpression of the multidrug efflux pumps MexCD-OprJ and MexEF-OprN is associated with a reduction of type III secretion in Pseudomonas aeruginosa. J. Bacteriol. 2005, 187, 1384-1391.
65. Hovey, A. K.; Frank, D. W. Analyses of the DNA-binding and transcriptional activation properties of ExsA, the transcriptional activator of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 1995, 177, 4427-4436.
66. Baucheron, S.; Imberechts, H.; Chaslus-Dancla, E.; Cloeckaert, A. The AcrB multidrug transporter plays a major role in high-level fluoroquinolone resistance in Salmonella enterica serovar typhimurium phage type DT204. Microb. Drug Resist. 2002, 8, 281-289.
67. Buckley, A. M.; Webber, M. A.; Cooles, S.; Randall, L. P.; La Ragione, R. M.; Woodward, M. J.; Piddock, L. J. V. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell Microbiol. 2006, 8, 847-856.
68. Shafer, W. M.; Qu, X.-D.; Waring, A. J.; Lehrer, R. I. Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc. Natl. Acad. Sci. USA 1998, 95, 1829-1833.
69. Fang, F. C. Antimicrobial reactive oxygen and nitrogen species: Concepts and controversies. Nat. Rev. Microbiol. 2004, 2, 820-832.
70. Koutsolioutsou, A.; Pena-Llopis, S.; Demple, B. Constitutive soxR mutations contribute to multiple-antibiotic resistance in clinical Escherichia coli isolates. Antimicrob. Agents Chemother. 2005, 49, 2746-2752.
71. Koutsolioutsou, A.; Martins, E. A.; White, D. G.; Levy, S. B.; Demple, B. A soxRS-constitutive mutation contributing to antibiotic resistance in a clinical isolate of Salmonella enterica (Serovar Typhimurium). Antimicrob. Agents Chemother. 2001, 45, 38-43.
72. Bratu, S.; Landman, D.; George, A.; Salvani, J.; Quale, J., Correlation of the expression of acrB and the regulatory genes marA, soxS and ramA with antimicrobial resistance in clinical isolates of Klebsiella pneumoniae endemic to New York City. J. Antimicrob. Chemother. 2009, 64, 278-283.
73. Pérez, A.; Poza, M.; Aranda, J.; Latasa, C.; Medrano, F. J.; Tomás, M.; Romero, A.; Lasa, I.; Bou, G. Effect of transcriptional activators SoxS, RobA, and RamA on expression of multidrug efflux pump AcrAB-TolC in Enterobacter cloacae. Antimicrob. Agents Chemother. 2012, 56, 6256-6266.
74. Jeannot, K.; Sobel, M. L.; El Garch, F.; Poole, K.; Plesiat, P. Induction of the MexXY efflux pump in Pseudomonas aeruginosa is dependent on drug-ribosome interaction. J. Bacteriol. 2005, 187, 5341-5346.
75. Vaisman, N.; Kerasin, E.; Hahn, T.; Trifon, S.; Voet, H.; Tabachnik, E. Increased neutrophil chemiluminescence production in patients with cystic fibrosis. Metab. Clin. Exp. 1994, 43, 719-722.
76. Vettoretti, L.; Plesiat, P.; Muller, C.; El Garch, F.; Phan, G.; Attree, I.; Ducruix, A.; Llanes, C. Efflux unbalance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob. Agents Chemother. 2009, 53, 1987-1997.
77. Ratjen, F.; Brockhaus, F.; Angyalosi, G. Aminoglycoside therapy against Pseudomonas aeruginosa in cystic fibrosis: A review. J. Cystic Fibros. 2009, 8, 361-369.
78. Jo, Y.-L.; Nara, F.; Ichihara, S.; Mizuno, T.; Mizushima, S. Purification and charcterization of the OmpR protein, a positive regulator involved in osmoregulatory expression of the ompF and ompC genes in Escherichia coli. J. Biol. Chem. 1986, 261, 15252-15256.
79. Lin, J.; Sahin, O.; Michel, L. O.; Zhang, Q. Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect. Immun. 2003, 71, 4250-4259.
80. Poole, K. Bacterial stress responses as determinants of antimicrobial resistance. J. Antimicrob. Chemother. 2012, 67, 2069-2089.
81. Nair, B. M.; Cheung, K. J.; Griffith, A.; Burns, J. L. Salicylate induces an antibiotic efflux pump in Burkholderia cepacia complex genomovar III (B. cenocepacia). J. Clin. Invest. 2004, 113, 464-473.
82. Kumar, A.; Chua, K. L.; Schweizer, H. P. Method for regulated expression of single-copy efflux pump genes in a surrogate Pseudomonas aeruginosa strain: Identification of the BpeEF-OprC chloramphenicol and trimethoprim efflux pump of Burkholderia pseudomallei 1026b. Antimicrob. Agents Chemother. 2006, 50, 3460-3463.
83. Coyne, S.; Rosenfeld, N.; Lambert, T.; Courvalin, P.; Perichon, B. Overexpression of resistance-nodulation-cell division pump AdeFGH confers multidrug resistance in Acinetobacter baumannii. Antimicrob. Agents Chemother. 2010, 54, 4389-4393.
84. Cortez-Cordova, J.; Kumar, A. Activity of the efflux pump inhibitor phenylalanine-arginine beta-naphthylamide against the AdeFGH pump of Acinetobacter baumannii. Int. J. Antimicrob. Agents 2011, 37, 420-424.
85. Schweizer, H. P. Colorado State University, Fort Collins, CO, USA. Personal communication, 2013.
86. Lynch, S. V.; Dixon, L.; Benoit, M. R.; Brodie, E. L.; Keyhan, M.; Hu, P.; Ackerley, D. F.; Andersen, G. L.; Matin, A. Role of the rapA Gene in controlling antibiotic resistance of Escherichia coli biofilms. Antimicrob. Agents Chemother. 2007, 51, 3650-3658.
87. Costerton, J. W.; Lewandowski, Z.; Caldwell, D. E.; Korber, D. R.; Lappin-Scott, H. M. Microbial biofilms. Annu. Rev. Microbiol. 1995, 49, 711-745.
88. Sandoz, K. M.; Mitzimberg, S. M.; Schuster, M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc. Natl. Acad. Sci. USA 2007, 104, 15876-15881.
89. Fuqua, C.; Greenberg, E. P. Listening in on bacteria: Acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 2002, 3, 685-695.
90. Houry, A.; Gohar, M.; Deschamps, J.; Tischenko, E.; Aymerich, S.; Gruss, A.; Briandet, R. Bacterial swimmers that infiltrate and take over the biofilm matrix. Proc. Natl. Acad. Sci. USA 2012, 109, 13088-13093.
91. De Kievit, T. R.; Parkins, M. D.; Gillis, R. J.; Srikumar, R.; Ceri, H.; Poole, K.; Iglewski, B. H.; Storey, D. G. Multidrug efflux pumps: Expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 2001, 45, 1761-1770.
92. Bratu, S.; Gupta, J.; Quale, J. Expression of the las and rhl quorum-sensing systems in clinical isolates of Pseudomonas aeruginosa does not correlate with efflux pump expression or antimicrobial resistance. J. Antimicrob. Chemother. 2006, 58, 1250-1253.
93. Gillis, R. J.; White, K. G.; Choi, K. H.; Wagner, V. E.; Schweizer, H. P.; Iglewski, B. H. Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 2005, 49, 3858-3867.
94. Southern, K. W.; Barker, P. M.; Solis-Moya, A.; Patel, L. Macrolide antibiotics for cystic fibrosis. Cochrane Database Syst. Rev. 2012, 11, doi: 10. 1002/14651858. CD002203. pub4.
95. Schaible, B.; Taylor, C. T.; Schaffer, K. Hypoxia increases antibiotic resistance in Pseudomonas aeruginosa through altering the composition of multidrug efflux pumps. Antimicrob. Agents Chemother. 2012, 56, 2114-2118.
96. Pamp, S. J.; Gjermansen, M.; Johansen, H. K.; Tolker-Nielsen, T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol. Microbiol. 2008, 68, 223-240.
97. Kvist, M.; Hancock, V.; Klemm, P. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl. Environ. Microbiol. 2008, 74, 7376-7382.
98. Couto, I.; Costa, S. S.; Viveiros, M.; Martins, M.; Amaral, L. Efflux-mediated response of Staphylococcus aureus exposed to ethidium bromide. Antimicrob. Agents Chemother. 2008, 62, 504-513.