Efflux-mediated resistance to a benzothiadiazol derivative effective against Burkholderia cenocepacia

Frontiers in Microbiology

Volumn 6, Issue AUG, 2015, Pages

  Scoffone, Viola C ^a   Ryabova, Olga ^b   Makarov, Vadim ^b   Iadarola, Paolo ^a   Fumagalli, Marco ^a   Fondi, Marco ^c   Fani, Renato ^c   Rossi, Edda De ^a   Riccardi, Giovanna ^a   Buroni, Silvia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b BACH INSTITUTE OF BIOCHEMISTRY   (Russian Federation)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Burkholderia; Cystic fibrosis; Drug resistance; Efflux pumps; Gram negatives; New antimicrobials

Indexed keywords

BENZOTHIADIAZOLE DERIVATIVE; CHLORAMPHENICOL; CIPROFLOXACIN; GENOMIC DNA; LEVOFLOXACIN; METHYL [(4 NITRO 2,1,3 BENZOTHIADIAZOL 5 YL) THIO] ACETATE; NALIDIXIC ACID; NORFLOXACIN; SPARFLOXACIN; THIADIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIUM ISOLATION; BACTERIUM MUTANT; BURKHOLDERIA CENOCEPACIA; COLONY FORMING UNIT; DNA EXTRACTION; HUMAN; HUMAN CELL; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PURIFICATION; SINGLE NUCLEOTIDE POLYMORPHISM; SPECTROPHOTOMETRY; TRANSCRIPTION REGULATION;

EID: 84940983414     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00815     Document Type: Article

References (31)

1. Aaron, S. D., Ferris, W., Henry, D. A., Speert, D. P., and Macdonald, N. E. (2000). Multiple combination bactericidal antibiotic testing for patients with cystic fibrosis infected with Burkholderia cepacia. Am. J. Respir. Crit. Care Med. 161, 1206-1212. doi: 10.1164/ajrccm.161.4.9907147
2. Bazzini, S., Udine, C., Sass, A., Pasca, M. R., Longo, F., Emiliani, G., et al. (2011). Deciphering the role of RND efflux transporters in Burkholderia cenocepacia. PLoS ONE 6:e18902. doi: 10.1371/journal.pone.0018902
3. Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., et al. (2014). SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42, W252-W258. doi: 10.1093/nar/gku340
4. Brown, N. L., Stoyanov, J. V., Kidd, S. P., and Hobman, J. L. (2003). The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27, 145-163. doi: 10.1016/S0168-6445(03)00051-2
5. Buroni, S., Matthijs, N., Spadaro, F., Van Acker, H., Scoffone, V. C., Pasca, M. R., et al. (2014). Differential role of RND efflux pumps in antimicrobial drug resistance of sessile and planktonic Burkholderia cenocepacia cells. Antimicrob. Agents Chemother. 58, 7424-7429. doi: 10.1128/AAC.03800-14
6. Buroni, S., Pasca, M. R., Flannagan, R. S., Bazzini, S., Milano, A., Bertani, I., et al. (2009). Assessment of three Resistance-Nodulation-Cell Division drug efflux transporters of Burkholderia cenocepacia in intrinsic antibiotic resistance. BMC Microbiol. 9:200. doi: 10.1186/1471-2180-9-200
7. Cardona, S., and Valvano, M. A. (2005). An expression vector containing a rhamnose-inducible promoter provides tightly regulated gene expression in Burkholderia cenocepacia. Plasmid 54, 219-228. doi: 10.1016/j.plasmid.2005.03.004
8. Chambers, J. R., and Sauer, K. (2013). The MerR-like regulator BrlR impairs Pseudomonas aeruginosa biofilm tolerance to colistin by repressing PhoPQ. J. Bacteriol. 195, 4678-4688. doi: 10.1128/JB.00834-13
9. Coenye, T., Van Acker, H., Peeters, E., Sass, A., Buroni, S., Riccardi, G., et al. (2011). Molecular mechanisms of chlorhexidine tolerance in Burkholderia cenocepacia biofilms. Antimicrob. Agents Chemother. 55, 1912-1919. doi: 10.1128/AAC.01571-10
10. Cox, M. P., Peterson, D. A., and Biggs, P. J. (2010). SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485. doi: 10.1186/1471-2105-11-485
11. Craig, F. F., Coote, J. G., Parton, R., Freer, J. H., and Gilmour, N. J. (1989). A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J. Gen. Microbiol. 135, 2885-2890. doi: 10.1099/00221287-135-11-2885
12. De Soyza, A., Meachery, G., Hester, K. L., Nicholson, A., Parry, G., Tocewicz, K., et al. (2010). Lung transplantation for patients with cystic fibrosis and Burkholderia cepacia complex infection: a single-center experience. J. Heart Lung Transplant. 9, 1395-1404. doi: 10.1016/j.healun.2010.06.007
13. Dodge, J. A., Lewis, P. A., Stanton, M., and Wilsher, J. (2007). Cystic fibrosis mortality and survival in the UK: 1947-2003. Eur. Respir. J. 29, 522-526. doi: 10.1183/09031936.00099506
14. Hidalgo, E., Ding, H., and Demple, B. (1997). Redox signal transduction: mutations shifting [2Fe-2S] centers of the SoxR sensor-regulator to the oxidized form. Cell 88, 121-129. doi: 10.1016/S0092-8674(00)81864-4
15. Higgins, C. F. (2007). Multiple molecular mechanisms for multidrug resistance transporters. Nature 446, 749-757. doi: 10.1038/nature05630
16. Horsley, A., Webb, K., Bright-Thomas, R., Govan, J., and Jones, A. (2011). Can early Burkholderia cepacia complex infection in cystic fibrosis be eradicated with antibiotic therapy? Front. Cell. Infect. Microbiol. 1:18. doi: 10.3389/fcimb.2011.00018
17. Koboldt, D. C., Chen, K., Wylie, T., Larson, D. E., McLellan, M. D., Mardis, E. R., et al. (2009). VarScan: variant detection in massively parallel sequencing of individual and pooled samples. Bioinformatics 25, 2283-2285. doi: 10.1093/bioinformatics/btp373
18. Lee, I. W., Levrelli, V., Park, S.-J., Totis, P. A., and Summers, A. O. (1993). In vivo DNA-protein interactions at the divergent mercury resistance (mer) promoters. J. Biol. Chem. 268, 2632-2639.
19. Lee, W. P., Stromberg, M. P., Ward, A., Stewart, C., Garrison, E. P., and Marth, G. T. (2014). MOSAIK: a hash-based algorithm for accurate next-generation sequencing short-read mapping. PLoS ONE 9:e90581. doi: 10.1371/journal.pone.0090581
20. LiPuma, J. J. (2010). The changing microbial epidemiology in cystic fibrosis. Clin. Microbiol. 23, 299-323. doi: 10.1128/CMR.00068-09
21. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
22. Martin, A., Takiff, H., Vandamme, P., Swings, J., Palomino, J. C., and Portaels, F. (2006). A new rapid and simple colorimetric method to detect pyrazinamide resistance in Mycobacterium tuberculosis using nicotinamide. J. Antimicrob. Chemother. 58, 327-331. doi: 10.1093/jac/dkl231
23. NCCLS. (1999). Methods for Determining Bactericidal Activity of Antimicrobial Agents: Approved Guideline M26-A. Wayne: National Committee for Clinical Laboratory Standards.
24. Noone, P. G. (2008). Lung transplant and cystic fibrosis: what's new from the UK and France? Thorax 63, 668-670. doi: 10.1136/thx.2008.099622
25. Perrin, E., Fondi, M., Papaleo, M. C., Maida, I., Emiliani, G., Buroni, S., et al. (2013). A census of RND superfamily proteins in the Burkholderia genus. Future Microbiol. 8, 923-937. doi: 10.2217/fmb.13.50
26. Quillardet, P., Huisman, O., D'Ari, R., and Hofnung, M. (1982). SOS chromotest, a direct assay of induction of an SOS function in Escherichia coli K-12 to measure genotoxicity. Proc. Natl. Acad. Sci. U.S.A. 79, 5971-5975. doi: 10.1073/pnas.79.19.5971
27. Saiman, L., Siegel, J., and Cystic Fibrosis Foundation. (2003). Infection control recommendations for patients with cystic fibrosis: microbiology, important pathogens, and infection control practices to prevent patient-to-patient transmission. Infect. Control. Hosp. Epidemiol. 24, S6-S52. doi: 10.1086/503485
28. Schmidtke, M., Schnittler, U., Jahn, B., Dahse, H., and Stelzner, A. (2001). A rapid assay for evaluation of antiviral activity against coxsackie virus B3, influenza virus A, and herpes simplex virus type 1. J. Virol. Methods 95, 133-143. doi: 10.1016/S0166-0934(01)00305-6
29. Scoffone, V. C., Spadaro, F., Udine, C., Makarov, V., Fondi, M., Fani, R., et al. (2014). Mechanism of resistance to an antitubercular 2-thiopyridine derivative that is also active against Burkholderia cenocepacia. Antimicrob. Agents Chemother. 58, 2415-2417. doi: 10.1128/AAC.02438-13
30. Silva, F., Lourenço, O., Queiroz, J. A., and Domingues, F. C. (2011). Bacteriostatic versus bactericidal activity of ciprofloxacin in Escherichia coli assessed by flow cytometry using a novel far-red dye. J. Antibiot. (Tokyo) 64, 321-325. doi: 10.1038/ja.2011.5
31. Watanabe, S., Kita, A., Kobayashi, K., and Miki, K. (2008). Crystal structure of the [2Fe-2S] oxidative-stress sensor SoxR bound to DNA. Proc. Natl. Acad. Sci. U.S.A. 105, 4121-4126. doi: 10.1073/pnas.0709188105