Protein modulator of multidrug efflux gene expression in Pseudomonas aeruginosa

Journal of Bacteriology

Volumn 189, Issue 15, 2007, Pages 5441-5451

  Daigle, Denis M ^b   Cao, Lily ^a   Fraud, Sebastien ^a   Wilke, Mark S ^c   Pacey, Angela ^a   Klinoski, Rachael ^a   Strynadka, Natalie C ^c   Dean, Charles R ^b   Poole, Keith ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MUTANT PROTEIN; PROTEIN ARMR; PROTEINM MEXR; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARMR GENE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; GENE MAPPING; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; ISOTHERMAL TITRATION CALORIMETRY; MEXA GENE; MEXAB GENE; NALC GENE; NONHUMAN; OPRM GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; TWO HYBRID SYSTEM;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT, ACTIVE; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PSEUDOMONAS AERUGINOSA; REPRESSOR PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 34547631283     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00543-07     Document Type: Article

References (69)

1. Adewoye, L., A. Sutherland, R. Srikumar, and K. Poole. 2002. The MexR repressor of the mexAB-oprM multidrug efflux operon in Pseudomonas aeruginosa: characterization of mutations compromising activity. J. Bacteriol. 184:4308-4312.
2. Aires, J. R., and H. Nikaido. 2005. Aminoglycosides are captured from both periplasm and cytoplasm by the AcrD multidrug efflux transporter of Escherichia coli. J. Bacteriol. 187:1923-1929.
3. Alekshun, M. N., and S. B. Levy. 1999. Alteration of the repressor activity of MarR, the negative regulator of the Escherichia coli marRAB locus, by multiple chemicals in vitro. J. Bacteriol. 181:4669-4672.
4. Alekshun, M. N., S. B. Levy, T. R. Mealy, B. A. Seaton, and J. F. Head. 2001. The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3 Å resolution. Nat. Struct. Biol. 8:710-714.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1992. Short protocols in molecular biology, 2nd ed. John Wiley & Sons, Inc., New York, NY.
6. Bai, U., I. Mandic-Mulec, and I. Smith. 1993. SinI modulates the activity of SinR, a developmental switch protein of Bacillus subtilis, by protein-protein interaction. Genes Dev. 7:139-148.
7. Barcak, G. J., M. S. Chandler, R. J. Redfield, and J. F. Tomb. 1991. Genetic systems in Haemophilus influenzae. Methods Enzymol. 204:321-342.
8. Cao, L., R. Srikumar, and K. Poole. 2004. MexAB-OprM hyperexpression in NalC type multidrug resistant Pseudomonas aeruginosa: identification and characterization of the nalC gene encoding a repressor of PA3720-PA3719. Mol. Microbiol. 53:1423-1436.
9. Choi, K. H., A. Kumar, and H. P. Schweizer. 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.
10. Chuanchuen, R., R. R. Karkhoff-Schweizer, and H. P. Schweizer. 2003. High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am. J. Infect. Control 31:124-127.
11. Core, L., and M. Perego. 2003. TPR-mediated interaction of RapC with ComA inhibits response regulator-DNA binding for competence development in Bacillus subtilis. Mol. Microbiol. 49:1509-1522.
12. Dmitrova, M., G. Younes-Cauet, P. Oertel-Buchheit, D. Porte, M. Schnarr, and M. Granger-Schnarr. 1998. A new LexA-based genetic system for monitoring and analyzing protein heterodimerization in Escherichia coli. Mol. Gen. Genet. 257:205-212.
13. Evans, K., L. Adewoye, and K. Poole. 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.
14. Evans, K., L. Passador, R. Srikumar, E. Tsang, J. Nezezon, and K. Poole. 1998. Influence of the MexAB-OprM multidrug efflux system on quorum-sensing in Pseudomonas aeruginosa. J. Bacteriol. 180:5443-5447.
15. Galan, B., A. Kolb, J. M. Sanz, J. L. Garcia, and M. A. Prieto. 2003. Molecular determinants of the hpa regulatory system of Escherichia coli: the HpaR repressor. Nucleic Acids Res. 31:6598-6609.
16. Galinier, A., J. Deutscher, and I. Martin-Verstraete. 1999. Phosphorylation of either Crh or HPr mediates binding of CcpA to the Bacillus subtilis xyn cre and catabolite repression of the xyn operon. J. Mol. Biol. 286:307-314.
17. Gorham, H. C., S. J. McGowan, P. R. Robson, and D. A. Hodgson. 1996. Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol. Microbiol. 19:171-186.
18. Hirakata, Y., R. Srikumar, K. Poole, N. Gotoh, T. Suematsu, S. Kohno, S. Kamihira, R. E. Hancock, and D. P. Speert. 2002. Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J. Exp. Med. 196:109-118.
19. Hong, M., M. Fuangthong, J. D. Helmann, and R. G. Brennan. 2005. Structure of an OhrR-ohrA operator complex reveals the DNA binding mechanism of the MarR family. Mol. Cell 20:131-141.
20. Jalal, S., and B. Wretlind. 1998. Mechanisms of quinolone resistance in clinical strains of Pseudomonas aeruginosa. Microb. Drug Resist. 4:257-261.
21. Jo, J. T., F. S. Brinkman, and R. E. Hancock. 2003. Aminoglycoside efflux in Pseudomonas aeruginosa: involvement of novel outer membrane proteins. Antimicrob. Agents Chemother. 47:1101-1111.
22. Jones, B. E., V. Dossonnet, E. Kuster, W. Hillen, J. Deutscher, and R. E. Klevit. 1997. Binding of the catabolite repressor protein CcpA to its DNA target is regulated by phosphorylation of its corepressor HPr. J. Biol. Chem. 272:26530-26535.
23. Keen, N. T., S. Tamaki, D. Kobayashi, and D. Trollinger. 1988. Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70:191-197.
24. Lei, S., L. Pulakat, and N. Gavini. 1999. Genetic analysis of nif regulatory genes by utilizing the yeast two-hybrid system detected formation of a NifL-NifA complex that is implicated in regulated expression of nif genes. J. Bacteriol. 181:6535-6539.
25. Li, X. Z., K. Poole, and H. Nikaido. 2003. Contributions of MexAB-OprM and an EmrE homologue to intrinsic resistance of Pseudomonas aeruginosa to aminoglycosides and dyes. Antimicrob. Agents Chemother. 47:27-33.
26. Li, X. Z., L. Zhang, and K. Poole. 1998. Role of the multidrug efflux systems of Pseudomonas aeruginosa in organic solvent tolerance. J. Bacteriol. 180:2987-2991.
27. Li, X. Z., and K. Poole. 1999. Organic solvent-tolerant mutants of Pseudomonas aeruginosa display multiple antibiotic resistance. Can. J. Microbiol. 45:18-22.
28. Lim, D., K. Poole, and N. C. Strynadka. 2002. Crystal structure of the MexR repressor from the multidrug efflux operon in Pseudomonas aeruginosa. J. Biol. Chem. 277:29253-29259.
29. Llanes, C., D. Hocquet, C. Vogne, D. Benali-Baitich, C. Neuwirth, and P. Plesiat. 2004. Clinical strains of Pseudomonas aeruginosa overproducing MexAB-OprM and MexXY efflux pumps simultaneously. Antimicrob. Agents Chemother. 48:1797-1802.
30. Lopez-Rubio, J. J., M. Elias-Arnanz, S. Padmanabhan, and F. J. Murillo. 2002. A repressor-antirepressor pair links two loci controlling light-induced carotenogenesis in Myxococcus xanthus. J. Biol. Chem. 277:7262-7270.
31. Martinez-Argudo, I., R. Little, N. Shearer, P. Johnson, and R. Dixon. 2004. The NifL-NifA system: a multidomain transcriptional regulatory complex that integrates environmental signals. J. Bacteriol. 186:601-610.
32. Masuda, N., and S. Ohya. 1992. Cross-resistance to meropenem, cephems, and quinolones in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 36:1847-1851.
33. Masuda, S., and C. E. Bauer. 2002. AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613-623.
34. McGowan, S. J., H. C. Gorham, and D. A. Hodgson. 1993. Light-induced carotenogenesis in Myxococcus xanthus: DNA sequence analysis of the carR region. Mol. Microbiol. 10:713-735.
35. Miller, J. H. 1992. A short course in bacterial genetics. A laboratory manual and handbook for Escherichia coli and related bacteria, p. 72-74. Cold Spring Harbor Laboratory Press, Plainview, NY.
36. Mima, T., H. Sekiya, T. Mizushima, T. Kuroda, and T. Tsuchiya. 2005. Gene cloning and properties of the RND-type multidrug efflux pumps MexPQ-OpmE and MexMN-OprM from Pseudomonas aeruginosa. Microbiol. Immunol. 49:999-1002.
37. Money, T., T. Jones, R. Dixon, and S. Austin. 1999. Isolation and properties of the complex between the enhancer binding protein NifA and the sensor NifL. J. Bacteriol. 181:4461-4468.
38. Morales, V. M., A. Backman, and M. Bagdasarian. 1991. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97:39-47.
39. Morita, Y., L. Cao, G. Gould, M. B. Avison, and K. Poole. 2006. nalD encodes a second repressor of the mexAB-oprM multidrug efflux operon of Pseudomonas aeruginosa. J. Bacteriol. 188:8649-8654.
40. Murakami, S., and A. Yamaguchi. 2003. Multidrug-exporting secondary transporters. Curr. Opin. Struct. Biol. 13:443-452.
41. Orth, P., D. Schnappinger, W. Hillen, W. Saenger, and W. Hinrichs. 2000. Structural basis of gene regulation by the tetracycline inducible Tet repressor-operator system. Nat. Struct. Biol. 7:215-219.
42. Palmer, M. 2003. Efflux of cytoplasmically acting antibiotics from gram-negative bacteria: periplasmic substrate capture by multicomponent efflux pumps inferred from their cooperative action with single-component transporters. J. Bacteriol. 185:5287-5289.
43. Pearson, J. P., C. Van Delden, and B. H. Iglewski. 1999. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J. Bacteriol. 181:1203-1210.
44. Perez-Marin, M. C., J. J. Lopez-Rubio, F. J. Murillo, M. Elias-Arnanz, and S. Padmanabhan. 2004. The N terminus of Myxococcus xanthus CarA repressor is an autonomously folding domain that mediates physical and functional interactions with both operator DNA and antirepressor protein. J. Biol. Chem. 279:33093-33103.
45. Poole, K. 2001. Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. J. Mol. Microbiol. Biotechnol. 3:255-264.
46. Poole, K. 2004. Efflux pumps, p. 635-674. In J.-L. Ramos (ed.), Pseudomonas, vol. I. Genomics, life style and molecular architecture. Kluwer Academic/Plenum Publishers, New York, NY.
47. Poole, K. 2004. Efflux-mediated multiresistance in Gram-negative bacteria. Clin. Microbiol. Infect. 10:12-26.
48. Poole, K. 2005. Efflux-mediated antimicrobial resistance 2007. J. Antimicrob. Chemother. 56:20-51.
49. Poole, K. p. 304-324. Antimicrobial and stress resistance. In M. Ehrmann (ed.), The periplasm. ASM Press, Washington, DC.
50. Poole, K., K. Tetro, Q. Zhao, S. Neshat, D. Heinrichs, and N. Bianco. 1996. Expression of the multidrug resistance operon mexA-mexB-oprM in Pseudomonas aeruginosa: mexR encodes a regulator of operon expression. Antimicrob. Agents Chemother. 40:2021-2028.
51. Providenti, M. A., and R. C. Wyndham. 2001. Identification and functional characterization of CbaR, a MarR-like modulator of the cbaABC-encoded chlorobenzoate catabolism pathway. Appl. Environ. Microbiol. 67:3530-3541.
52. Redly, A., and K. Poole. 2003. Pyoverdine-mediated regulation of FpvA synthesis in Pseudomonas aeruginosa: involvement of a probable ECF sigma factor, FpvI. J. Bacteriol. 185:1261-1265.
53. Redly, G. A., and K. Poole. 2005. FpvIR control of fpvA ferric pyoverdine receptor gene expression in Pseudomonas aeruginosa: demonstration of an interaction between FpvI and FpvR and identification of mutations in each compromising this interaction. J. Bacteriol. 187:5648-5657.
54. Saito, K., S. Eda, H. Maseda, and T. Nakae. 2001. Molecular mechanism of MexR-mediated regulation of MexAB-OprM efflux pump expression in Pseudomonas aeruginosa. FEMS Microbiol. Lett. 195:23-28.
55. Saito, K., H. Yoneyama, and T. Nakae. 1999. 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. 179:67-72.
56. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
57. Sanchez, P., F. Rojo, and J. L. Martinez. 2002. Transcriptional regulation of mexR, the repressor of Pseudomonas aeruginosa mexAB-oprM multidrug efflux pump. FEMS Microbiol. Lett. 207:63-68.
58. Schweizer, H. P. 1998. Intrinsic resistance to inhibitors of fatty acid biosynthesis in Pseudomonas aeruginosa is due to efflux: application of a novel technique for generation of unmarked chromosomal mutations for the study of efflux systems. Antimicrob. Agents Chemother. 42:394-398.
59. Sheu, D. S., Y. T. Wang, and C. Y. Lee. 2000. Rapid detection of polyhydroxyalkanoate-accumulating bacteria isolated from the environment by colony PCR. Microbiology 146:2019-2025.
60. Sobel, M. L., D. Hocquet, L. Cao, P. Plesiat, and K. Poole. 2005. Mutations in PA3574 (nalD) lead to increased MexAB-OprM expression and multidrug resistance in lab and clinical isolates of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 49:1782-1786.
61. Srikumar, R., T. Kon, N. Gotoh, and K. Poole. 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.
62. Srikumar, R., X.-Z. Li, and K. Poole. 1997. Inner membrane efflux components are responsible for the β-lactam specificity of multidrug efflux pumps in Pseudomonas aeruginosa. J. Bacteriol. 179:7875-7881.
63. Srikumar, R., C. J. Paul, and K. Poole. 2000. Influence of mutations in the mexR repressor gene on expression of the MexA-MexB-OprM multidrug efflux system of Pseudomonas aeruginosa. J. Bacteriol. 182:1410-1414.
64. Srikumar, R., and K. Poole. 1999. Demonstration of ethidium bromide efflux by multiresistant pumps of Pseudomonas aeruginosa. Clin. Microbiol. Infect. 5:5S58-5S59.
65. van Aalten, D. M., C. C. DiRusso, and J. Knudsen. 2001. The structural basis of acyl coenzyme A-dependent regulation of the transcription factor FadR. EMBO J. 20:2041-2050.
66. Whitworth, D. E., and D. A. Hodgson. 2001. Light-induced carotenogenesis in Myxococcus xanthus: evidence that CarS acts as an anti-repressor of CarA. Mol. Microbiol. 42:809-819.
67. Wilkinson, S. P., and A. Grove. 2004. HucR, a novel uric acid-responsive member of the MarR family of transcriptional regulators from Deinococcus radiodurans. J. Biol. Chem. 279:51442-51450.
68. Wilkinson, S. P., and A. Grove. 2006. Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Curr. Issues Mol. Biol. 8:51-62.
69. Zhao, Q., X.-Z. Li, R. Srikumar, and K. Poole. 1998. Contribution of outer membrane efflux protein OprM to antibiotic resistance in Pseudomonas aeruginosa independent of MexAB. Antimicrob. Agents Chemother. 42:1682-1688.