The NfxB repressor of the mexCD-oprJ multidrug efflux operon of Pseudomonas aeruginosa

Microbiology (United Kingdom)

Volumn 159, Issue PART 10, 2013, Pages 2058-2073

  Purssell, Andrew ^a   Poole, Keith ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL STRAIN; BINDING AFFINITY; BINDING SITE; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; DNA BINDING; EFFUSION; GEL PERMEATION CHROMATOGRAPHY; GENE EXPRESSION; GENE FUNCTION; MULTIDRUG RESISTANCE; NFXB REPRESSOR; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PSEUDOMONAS AERUGINOSA; REPRESSOR GENE; SITE DIRECTED MUTAGENESIS; WILD TYPE; BIOSYNTHESIS; GEL CHROMATOGRAPHY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; TWO HYBRID SYSTEM;

BACTERIAL DNA; BACTERIAL PROTEIN; CARRIER PROTEIN; DNA BINDING PROTEIN; MEMBRANE PROTEIN; MEXC PROTEIN, PSEUDOMONAS AERUGINOSA; MEXD PROTEIN, PSEUDOMONAS AERUGINOSA; NFXB PROTEIN, PSEUDOMONAS AERUGINOSA; OPRJ PROTEIN, PSEUDOMONAS AERUGINOSA; TRANSCRIPTION FACTOR; PROTEIN BINDING;

BACTERIAL PROTEINS; CHROMATOGRAPHY, GEL; DNA MUTATIONAL ANALYSIS; DNA, BACTERIAL; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PSEUDOMONAS AERUGINOSA; TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84884811030     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.069286-0     Document Type: Article

References (71)

1. Alberti, S., Oehler, S., von Wilcken-Bergmann, B., Krämer, H. & Müller-Hill, B. (1991). Dimer-to-tetramer assembly of Lac repressor involves a leucine heptad repeat. New Biol 3, 57-62.
2. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. (2006). The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201.
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1992). Short Protocols in Molecular Biology, 2nd edn. New York: Wiley.
4. Benkert, P., Tosatto, S. C. & Schomburg, D. (2008). QMEAN: a comprehensive scoring function for model quality assessment. Proteins 71, 261-277.
5. 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. & other authors (2012). Mechanisms decreasing in vitro susceptibility to the LpxC inhibitor CHIR-090 in the Gram-negative pathogen Pseudomonas aeruginosa. Antimicrob Agents Chemother 56, 17-27.
6. Chiang, W. C., Pamp, S. J., Nilsson, M., Givskov, M. & Tolker-Nielsen, T. (2012). The metabolically active subpopulation in Pseudomonas aeruginosa biofilms survives exposure to membrane-targeting antimicrobials via distinct molecular mechanisms. FEMS Immunol Med Microbiol 65, 245-256.
7. Choi, K. H. & Schweizer, H. P. (2005). An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol 5, 30.
8. Choi, K. H., Kumar, A. & Schweizer, H. P. (2006). A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64, 391-397.
9. Christen, M., Hünenberger, P. H., Bakowies, D., Baron, R., Bürgi, R., Geerke, D. P., Heinz, T. N., Kastenholz, M. A., Kräutler, V. & other authors (2005). The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem 26, 1719-1751.
10. Chuanchuen, R., Beinlich, K., Hoang, T. T., Becher, A., Karkhoff-Schweizer, R. R. & Schweizer, H. P. (2001). 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 45, 428-432.
11. Daddaoua, A., Krell, T. & Ramos, J. L. (2009). Regulation of glucose metabolism in Pseudomonas: the phosphorylative branch and Entner-Doudoroff enzymes are regulated by a repressor containing a sugar isomerase domain. J Biol Chem 284, 21360-21368.
12. Dean, C. R., Visalli, M. A., Projan, S. J., Sum, P. E. & Bradford, P. A. (2003). Efflux-mediated resistance to tigecycline (GAR-936) in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 47, 972-978.
13. Dimitrova, M., Younès-Cauet, G., Oertel-Buchheit, P., Porte, D., Schnarr, M. & Granger-Schnarr, M. (1998). A new LexA-based genetic system for monitoring and analyzing protein heterodimerization in Escherichia coli. Mol Gen Genet 257, 205-212.
14. Dong, F., Spott, S., Zimmermann, O., Kisters-Woike, B., Müller-Hill, B. & Barker, A. (1999). Dimerisation mutants of lac repressor. I. A monomeric mutant, L251A, that binds lac operator DNA as a dimer. J Mol Biol 290, 653-666.
15. Esbelin, J., Jouanneau, Y., Armengaud, J. & Duport, C. (2008). ApoFnr binds as a monomer to promoters regulating the expression of enterotoxin genes of Bacillus cereus. J Bacteriol 190, 4242-4251.
16. Evans, K., Adewoye, L. & Poole, K. (2001). MexR repressor of the mexAB-oprM multidrug efflux operon of Pseudomonas aeruginosa: identification of MexR binding sites in the mexA-mexR intergenic region. J Bacteriol 183, 807-812.
17. Fraud, S., Campigotto, A. J., Chen, Z. & Poole, K. (2008). MexCDOprJ multidrug efflux system of Pseudomonas aeruginosa: involvement in chlorhexidine resistance and induction by membranedamaging agents dependent upon the AlgU stress response sigma factor. Antimicrob Agents Chemother 52, 4478-4482.
18. Gillis, R. J., White, K. G., Choi, K. H., Wagner, V. E., Schweizer, H. P. & Iglewski, B. H. (2005). Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 49, 3858-3867.
19. Henrichfreise, B., Wiegand, I., Pfister, W. & Wiedemann, B. (2007). Resistance mechanisms of multiresistant Pseudomonas aeruginosa strains from Germany and correlation with hypermutation. Antimicrob Agents Chemother 51, 4062-4070.
20. E). Proc Natl Acad Sci U S A 92, 7941-7945.
21. Higgins, P. G., Fluit, A. C., Milatovic, D., Verhoef, J. & Schmitz, F. J. (2003). Mutations in GyrA, ParC, MexR and NfxB in clinical isolates of Pseudomonas aeruginosa. Int J Antimicrob Agents 21, 409-413.
22. Hirai, K., Suzue, S., Irikura, T., Iyobe, S. & Mitsuhashi, S. (1987). Mutations producing resistance to norfloxacin in Pseudomonas aeruginosa. Antimicrob Agents Chemother 31, 582-586.
23. Hirakata, Y., Srikumar, R., Poole, K., Gotoh, N., Suematsu, T., Kohno, S., Kamihira, S., Hancock, R. E. & Speert, D. P. (2002). Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J Exp Med 196, 109-118.
24. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J. & Schweizer, H. P. (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.
25. Hohnadel, D., Haas, D. & Meyer, J.-M. (1986). Mapping of mutations affecting pyoverdine production in Pseudomonas aeruginosa. FEMS Microbiol Lett 36, 195-199.
26. Jakics, E. B., Iyobe, S., Hirai, K., Fukuda, H. & Hashimoto, H. (1992). Occurrence of the nfxB type mutation in clinical isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother 36, 2562-2565.
27. Jalal, S. & Wretlind, B. (1998). Mechanisms of quinolone resistance in clinical strains of Pseudomonas aeruginosa. Microb Drug Resist 4, 257-261.
28. Jalal, S., Ciofu, O., Hoiby, N., Gotoh, N. & Wretlind, B. (2000). Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Antimicrob Agents Chemother 44, 710-712.
29. Jeannot, K., Elsen, S., Köhler, T., Attree, I., van Delden, C. & Plésiat, P. (2008). Resistance and virulence of Pseudomonas aeruginosa clinical strains overproducing the MexCD-OprJ efflux pump. Antimicrob Agents Chemother 52, 2455-2462.
30. Jo, J. T., Brinkman, F. S. & Hancock, R. E. (2003). Aminoglycoside efflux in Pseudomonas aeruginosa: involvement of novel outer membrane proteins. Antimicrob Agents Chemother 47, 1101-1111.
31. Join-Lambert, O. F., Michéa-Hamzehpour, M., Köhler, T., Chau, F., Faurisson, F., Dautrey, S., Vissuzaine, C., Carbon, C. & Pechère, J. C. (2001). Differential selection of multidrug efflux mutants by trovafloxacin and ciprofloxacin in an experimental model of Pseudomonas aeruginosa acute pneumonia in rats. Antimicrob Agents Chemother 45, 571-576.
32. Kim, B. & Little, J. W. (1992). Dimerization of a specific DNA-binding protein on the DNA. Science 255, 203-206.
33. Kiser, T. H., Obritsch, M. D., Jung, R., MacLaren, R. & Fish, D. N. (2010). Efflux pump contribution to multidrug resistance in clinical isolates of Pseudomonas aeruginosa. Pharmacotherapy 30, 632-638.
34. Köhler, T., Michea-Hamzehpour, M., Plesiat, P., Kahr, A. L. & Pechere, J. C. (1997). Differential selection of multidrug efflux systems by quinolones in Pseudomonas aeruginosa. Antimicrob Agents Chemother 41, 2540-2543.
35. Lewis, M., Chang, G., Horton, N. C., Kercher, M. A., Pace, H. C., Schumacher, M. A., Brennan, R. G. & Lu, P. (1996). Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 271, 1247-1254.
36. Li, X. Z., Zhang, L. & Poole, K. (1998). Role of the multidrug efflux systems of Pseudomonas aeruginosa in organic solvent tolerance. J Bacteriol 180, 2987-2991.
37. Lu, D., Fillet, S., Meng, C., Alguel, Y., Kloppsteck, P., Bergeron, J., Krell, T., Gallegos, M. T., Ramos, J. & Zhang, X. (2010). Crystal structure of TtgV in complex with its DNA operator reveals a general model for cooperative DNA binding of tetrameric gene regulators. Genes Dev 24, 2556-2565.
38. Mandsberg, L. F., Maciá, M. D., Bergmann, K. R., Christiansen, L. E., Alhede, M., Kirkby, N., Høiby, N., Oliver, A. & Ciofu, O. (2011). Development of antibiotic resistance and up-regulation of the antimutator gene pfpI in mutator Pseudomonas aeruginosa due to inactivation of two DNA oxidative repair genes (mutY, mutM). FEMS Microbiol Lett 324, 28-37.
39. Martin, D. W., Holloway, B. W. & Deretic, V. (1993). Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J Bacteriol 175, 1153-1164.
40. Masuda, N. & Ohya, S. (1992). Cross-resistance to meropenem, cephems, and quinolones in Pseudomonas aeruginosa. Antimicrob Agents Chemother 36, 1847-1851.
41. Masuda, N., Sakagawa, E. & Ohya, S. (1995). Outer membrane proteins responsible for multiple drug resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 39, 645-649.
42. Masuda, N., Sakagawa, E., Ohya, S., Gotoh, N., Tsujimoto, H. & Nishino, T. (2000). Substrate specificities of MexAB-OprM, MexCDOprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 44, 3322-3327.
43. Miller, J. H. (1992). A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Plainview, NY: Cold Spring Harbour Laboratory.
44. Monferrer, D., Tralau, T., Kertesz, M. A., Dix, I., Solà, M. & Usón, I. (2010). Structural studies on the full-length LysR-type regulator TsaR from Comamonas testosteroni T-2 reveal a novel open conformation of the tetrameric LTTR fold. Mol Microbiol 75, 1199-1214.
45. Morita, Y., Murata, T., Mima, T., Shiota, S., Kuroda, T., Mizushima, T., Gotoh, N., Nishino, T. & Tsuchiya, T. (2003). Induction of mexCDoprJ operon for a multidrug efflux pump by disinfectants in wild-type Pseudomonas aeruginosa PAO1. J Antimicrob Chemother 51, 991-994.
46. Mulet, X., Maciá, M. D., Mena, A., Juan, C., Pérez, J. L. & Oliver, A. (2009). Azithromycin in Pseudomonas aeruginosa biofilms: bactericidal activity and selection of nfxB mutants. Antimicrob Agents Chemother 53, 1552-1560.
47. Muraoka, S., Okumura, R., Ogawa, N., Nonaka, T., Miyashita, K. & Senda, T. (2003). Crystal structure of a full-length LysR-type transcriptional regulator, CbnR: unusual combination of two subunit forms and molecular bases for causing and changing DNA bend. J Mol Biol 328, 555-566.
48. Nehme, D., Li, X. Z., Elliot, R. & Poole, K. (2004). Assembly of the MexAB-OprM multidrug efflux system of Pseudomonas aeruginosa: identification and characterization of mutations in mexA compromising MexA multimerization and interaction with MexB. J Bacteriol 186, 2973-2983.
49. Poole, K. (2000). Efflux-mediated resistance to fluoroquinolones in Gram-negative bacteria. Antimicrob Agents Chemother 44, 2233-2241.
50. Poole, K. (2011). Pseudomonas aeruginosa: resistance to the max. Front Microbiol 2, 65.
51. Poole, K. (2012). Efflux-mediated antimicrobial resistance. In Antibiotic Discovery and Development, pp. 349-395. Edited by T. J. Dougherty & M. J. Pucci. New York: Springer.
52. Poole, K., Gotoh, N., Tsujimoto, H., Zhao, Q., Wada, A., Yamasaki, T., Neshat, S., Yamagishi, J., Li, X. Z. & Nishino, T. (1996). Overexpression of the mexC-mexD-oprJ efflux operon in nfxB-type multidrug-resistant strains of Pseudomonas aeruginosa. Mol Microbiol 21, 713-725.
53. Rédly, G. A. & Poole, K. (2003). Pyoverdine-mediated regulation of FpvA synthesis in Pseudomonas aeruginosa: involvement of a probable extracytoplasmic-function sigma factor, FpvI. J Bacteriol 185, 1261-1265.
54. Reinhardt, A., Köhler, T., Wood, P., Rohner, P., Dumas, J. L., Ricou, B. & van Delden, C. (2007). Development and persistence of antimicrobial resistance in Pseudomonas aeruginosa: a longitudinal observation in mechanically ventilated patients. Antimicrob Agents Chemother 51, 1341-1350.
55. Rhee, J. E., Sheng, W., Morgan, L. K., Nolet, R., Liao, X. & Kenney, L. J. (2008). Amino acids important for DNA recognition by the response regulator OmpR. J Biol Chem 283, 8664-8677.
56. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
57. Sheu, D. S., Wang, Y. T. & Lee, C. Y. (2000). Rapid detection of polyhydroxyalkanoate-accumulating bacteria isolated from the environment by colony PCR. Microbiology 146, 2019-2025.
58. Shiba, T., Ishiguro, K., Takemoto, N., Koibuchi, H. & Sugimoto, K. (1995). Purification and characterization of the Pseudomonas aeruginosa NfxB protein, the negative regulator of the nfxB gene. J Bacteriol 177, 5872-5877.
59. Simon, R., Priefer, U. & Pühler, A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Nature Biotechnol 1, 784-791.
60. Singh, V., Ekka, M. K. & Kumaran, S. (2012). Second monomer binding is the rate-limiting step in the formation of the dimeric PhoP-DNA complex. Biochemistry 51, 1346-1356.
61. Sobel, M. L., McKay, G. A. & Poole, K. (2003). Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 47, 3202-3207.
62. Srikumar, R., Li, X. Z. & Poole, K. (1997). Inner membrane efflux components are responsible for β-lactam specificity of multidrug efflux pumps in Pseudomonas aeruginosa. J Bacteriol 179, 7875-7881.
63. Srikumar, R., Kon, T., Gotoh, N. & Poole, K. (1998). Expression of Pseudomonas aeruginosa multidrug efflux pumps MexA-MexB-OprM and MexC-MexD-OprJ in a multidrug-sensitive Escherichia coli strain. Antimicrob Agents Chemother 42, 65-71.
64. Starr, L. M., Fruci, M. & Poole, K. (2012). Pentachlorophenol induction of the Pseudomonas aeruginosa mexAB-oprM efflux operon: involvement of repressors NalC and MexR and the antirepressor ArmR. PLoS ONE 7, e32684.
65. Studier, F. W. (1991). Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system. J Mol Biol 219, 37-44.
66. Studier, F. W., Rosenberg, A. H., Dunn, J. J. & Dubendorff, J. W. (1990). Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185, 60-89.
67. Suckow, J., Markiewicz, P., Kleina, L. G., Miller, J., Kisters-Woike, B. & Müller-Hill, B. (1996). Genetic studies of the Lac repressor. XV: 4000 single amino acid substitutions and analysis of the resulting phenotypes on the basis of the protein structure. J Mol Biol 261, 509-523.
68. Yoshida, T., Muratani, T., Iyobe, S. & Mitsuhashi, S. (1994). Mechanisms of high-level resistance to quinolones in urinary tract isolates of Pseudomonas aeruginosa. Antimicrob Agents Chemother 38, 1466-1469.
69. E and Pseudomonas aeruginosa AlgU: E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa. J Bacteriol 177, 3259-3268.
70. Zhanel, G. G., Hoban, D. J., Schurek, K. & Karlowsky, J. A. (2004). Role of efflux mechanisms on fluoroquinolone resistance in Streptococcus pneumoniae and Pseudomonas aeruginosa. Int J Antimicrob Agents 24, 529-535.
71. Zhang, R. G., Kim, Y., Skarina, T., Beasley, S., Laskowski, R., Arrowsmith, C., Edwards, A., Joachimiak, A. & Savchenko, A. (2002). Crystal structure of Thermotoga maritima 0065, a member of the IclR transcriptional factor family. J Biol Chem 277, 19183-19190.