Deciphering the role of rnd efflux transporters in burkholderia cenocepacia

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Bazzini, Silvia ^a   Udine, Claudia ^a   Sass, Andrea ^b   Pasca, Maria Rosalia ^a   Longo, Francesca ^c   Emiliani, Giovanni ^d   Fondi, Marco ^e   Perrin, Elena ^e   Decorosi, Francesca ^e   Viti, Carlo ^e   Giovannetti, Luciana ^e   Leoni, Livia ^c   Fani, Renato ^e   Riccardi, Giovanna ^a   Mahenthiralingam, Eshwar ^b   Buroni, Silvia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c ROMA TRE UNIVERSITY   (Italy)

^d Trees and Timber Institute National Research Council   (Italy)

^e UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; AZTREONAM; CARRIER PROTEIN; CEFTAZIDIME; CHLORAMPHENICOL; CIPROFLOXACIN; ERYTHROMYCIN; ETHIDIUM BROMIDE; GENTAMICIN; KANAMYCIN; LEVOFLOXACIN; MEROPENEM; NALIDIXIC ACID; NORFLOXACIN; PIPERACILLIN; RESISTANCE NODULATION CELL DIVISION 4 EFFLUX TRANSPORTER; RESISTANCE NODULATION CELL DIVISION 9 EFFLUX TRANSPORTER; RESISTANCE NODULATION CELL DIVISION EFFLUX TRANSPORTER; SPARFLOXACIN; TOBRAMYCIN; TRIMETHOPRIM; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOFILM; BURKHOLDERIA CENOCEPACIA; CHEMOTAXIS; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; MORPHOLOGICAL TRAIT; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTOMICS; UPREGULATION; BACTERIUM ADHERENCE; DNA MICROARRAY; DRUG EFFECT; FLAGELLUM; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGICAL EXAMINATION; MOVEMENT (PHYSIOLOGY); OPERON; PHENOTYPE; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; REPRODUCIBILITY;

BURKHOLDERIA CENOCEPACIA; NEGIBACTERIA;

ANTI-INFECTIVE AGENTS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; BURKHOLDERIA CENOCEPACIA; CHEMOTAXIS; DOWN-REGULATION; DRUG RESISTANCE, BACTERIAL; FLAGELLA; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MOVEMENT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OPERON; PHENOTYPE; PRINCIPAL COMPONENT ANALYSIS; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79955435815     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018902     Document Type: Article

References (47)

1. LiPuma JJ, (2010) The changing microbial epidemiology in cystic fibrosis. Clin Microbiol Rev 23: 299-323.
2. Foweraker J, (2009) Recent advances in the microbiology of respiratory tract infection in cystic fibrosis. British Medical Bulletin 89: 93-110.
3. Mahenthiralingam E, Baldwin A, Dowson CG, (2008) Burkholderia cenocepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104: 1539-1551.
4. Cunha LG Jr, Assis MC, Machado GB, Assef AP, Marques EA, et al. (2010) Potential mechanisms underlying the acute lung dysfunction and bacterial extrapulmonary dissemination during Burkholderia cenocepacia respiratory infection. Respir Res 18: 11-14.
5. Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, et al. (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191: 261-277.
6. Peeters E, Nelis HJ, Coenye T, (2009) In vitro activity of ceftazidime, ciprofloxacin, meropenem, minocyclin, tobramycin and co-trimoxazole on planktonic and sessile Burkholderia cepacia complex bacteria. J Antimicrob Chemother 64: 801-809.
7. Saiman L, Siegel J, (2003) Cystic Fibrosis Foundation. 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: S6-52.
8. Nikaido H, Takatsuka Y, (2009) Mechanisms of RND multidrug efflux pumps. Biochem Biophys Acta 179: 769-781.
9. Akama H, Kanemaki M, Yoshimura M, Tsukihara T, Kashiwagi T, et al. (2004) 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 279: 52816-52819.
10. Akama H, Matsuura T, Kashiwagi S, Yoneyama H, Narita S, et al. (2004) Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J Biol Chem 279: 25939-25942.
11. Higgins MK, Bokma E, Koronakis E, Hughes C, Koronakis V, (2004) Structure of the periplasmic component of a bacterial drug efflux pump. Proc Natl Acad Sci USA 101: 9994-9999.
12. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C, (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405: 914-919.
13. Murakami S, Nakashima R, Yamashita E, Yamaguchi A, (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419: 587-593.
14. Piddock LJ, (2006) Multidrug-resistance efflux pumps - not just for resistance. Nat Rev Microbiol 4: 629-636.
15. Ma Z, Jacobsen FE, Giedroc DP, (2009) Coordination chemistry of bacterial metal transport and sensing. Chem Rev 109: 4644-4681.
16. Guglierame P, Pasca MR, De Rossi E, Buroni S, Arrigo P, et al. (2006) Efflux pump genes of the resistance-nodulation-division family in Burkholderia cenocepacia genome. BMC Microbiol 6: 66.
17. Perrin E, Fondi M, Papaleo MC, Maida I, Buroni S, et al. (2010) Exploring the HME and HAE1 efflux systems in the genus Burkholderia. BMC Evol Biol 10: 164.
18. Buroni S, Pasca MR, Flannagan RS, Bazzini S, Milano A, et al. (2009) Assessment of three Resistance-Nodulation-Cell Division drug efflux transporters of Burkholderia cenocepacia in intrinsic antibiotic resistance. BMC Microbiol 9: 200.
19. Flannagan RS, Linn T, Valvano MA, (2008) A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ Microbiol 10: 1652-1660.
20. Coenye T, Van Acker H, Peeters E, Sass A, Buroni S, et al. (2011) Molecular mechanisms of chlorhexidine tolerance in Burkholderia cenocepacia biofilms. Antimicrob Agents Chemother. In press.
21. Drevinek P, Holden MT, Ge Z, Jones AM, Ketchell I, et al. (2008) Gene expression changes linked to antimicrobial resistance, oxidative stress, iron depletion and retained motility are observed when Burkholderia cenocepacia grows in cystic fibrosis sputum. BMC Infect Dis 8: 121.
22. Köhler T, van Delden C, Curty LK, Hamzehpour MM, Pechere JC, (2001) Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa. J Bacteriol 183: 5213-5222.
23. Poole K, (2001) Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. J Mol Microbiol Biotechnol 3: 255-264.
24. Sambrook J, Russell DW, (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Cold Spring Harbor Laboratory Press.
25. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
26. Rose H, Baldwin A, Dowson CG, Mahenthiralingam E, (2009) Biocide susceptibility of the Burkholderia cepacia complex. J Antimicrob Chemother 63: 502-510.
27. Rampioni G, Schuster M, Greenberg EP, Zennaro E, Leoni L, (2009) Contribution of the RsaL global regulator to Pseudomonas aeruginosa virulence and biofilm formation. FEMS Microbiol Lett 301: 210-217.
28. Leungsakul T, Keenan BG, Smets BF, Wood TK, (2005) TNT and nitroaromatic compounds are chemoattractants for Burkholderia cepacia R34 and Burkholderia sp. strain DNT. Appl Microbiol Biotechnol 69: 321-325.
29. Bochner BR, Gadzinski P, Panomitros E, (2001) Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res 11: 1246-1255.
30. Mahenthiralingam E, Urban TA, Goldberg JB, (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156.
31. Moens S, Vanderleyden J, (1996) Functions of bacterial flagella. Crit Rev Microbiol 22: 67-100.
32. O'Toole GA, Kolter R, (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
33. Urban TA, Griffith A, Torok AM, Smolkin ME, Burns JL, et al. (2004) Contribution of Burkholderia cenocepacia flagella to infectivity and inflammation. Infect Immun 72: 5126-5134.
34. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, et al. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
35. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
36. Liaudet L, Szabo C, Evgenov OV, Murthy KG, Pacher P, et al. (2003) Flagellin from gram-negative bacteria is a potent mediator of acute pulmonary inflammation in sepsis. Shock 19: 131-137.
37. Hales BA, Morgan JA, Hart CA, Winstanley C, (1998) Variation in flagellin genes and proteins of Burkholderia cepacia. J Bacteriol 180: 1110-1118.
38. Montie TC, Stover GB, (1983) Isolation and characterization of flagellar preparations from Pseudomonas species. J Clin Microbiol 18: 452-456.
39. Hazelbauer GL, Falke JJ, Parkinson JS, (2008) Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9-19.
40. Hess JF, Oosawa K, Kaplan N, Simon MI, (1988) Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53: 79-87.
41. Silversmith RE, (2010) Auxiliary phosphatases in two-component signal transduction. Curr Opin Microbiol 13: 177-183.
42. Anderson JK, Smith TG, Hoover TR, (2010) Sense and sensibility: flagellum-mediated gene regulation. Trends Microbiol 18: 30-37.
43. Bochner BR, Giovannetti L, Viti C, (2008) Important discoveries from analysing bacterial phenotypes. Mol Microbiol 70: 274-280.
44. Peeters E, Sass A, Mahenthiralingam E, Nelis H, Coenye T, (2010) Transcriptional response of Burkholderia cenocepacia J2315 sessile cells to treatments with high doses of hydrogen peroxide and sodium hypochlorite. BMC Genomics 11: 90.
45. Webber MA, Bailey AM, Blair JM, Morgan E, Stevens MP, et al. (2009) The global consequence of disruption of the AcrAB-TolC efflux pump in Salmonella enterica includes reduced expression of SPI-1 and other attributes required to infect the host. J Bacteriol 191: 4276-4285.
46. Coenye T, (2010) Social interactions in the Burkholderia cepacia complex: biofilms and quorum sensing. Fut Microbiol 5: 1087-1099.
47. Coenye T, (2010) Response of sessile cells to stress: from changes in gene expression to phenotypic adaptation. FEMS Immunol Med Microbiol 59: 239-252.