Differential roles of rnd efflux pumps in antimicrobial drug resistance of sessile and planktonic burkholderia cenocepacia cells

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 12, 2014, Pages 7424-7429

  Buroni, Silvia ^a   Matthijs, Nele ^b   Spadaro, Francesca ^a   Van Acker, Heleen ^b   Scoffone, Viola C ^a   Pasca, Maria Rosalia ^a   Riccardi, Giovanna ^a   Coenye, Tom ^b  

^a UNIVERSITY OF PAVIA   (Italy)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORAMPHENICOL; CIPROFLOXACIN; DNA FRAGMENT; MEROPENEM; MINOCYCLINE; PROTEIN; RESISTANCE NODULATION CELL DIVISION PROTEIN; RESISTANCE NODULATION CELL DIVISION PROTEIN 3; RESISTANCE NODULATION CELL DIVISION PROTEIN 8; RESISTANCE NODULATION CELL DIVISION PROTEIN 9; TOBRAMYCIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CARRIER PROTEIN; MESSENGER RNA; OUTER MEMBRANE PROTEIN;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL; BACTERICIDAL ACTIVITY; BIOFILM; BURKHOLDERIA CENOCEPACIA; DRUG EFFECT; EFFUSION; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; INDEL MUTATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPERON; PLANKTON; QUANTITATIVE ANALYSIS; RESPIRATORY TRACT INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; SESSILE SPECIES; WILD TYPE; DRUG EFFECTS; GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR GENETICS; MULTIDRUG RESISTANCE; NUCLEOTIDE SEQUENCE;

ANTI-BACTERIAL AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; BIOFILMS; BURKHOLDERIA CENOCEPACIA; CIPROFLOXACIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, MDR; MEMBRANE TRANSPORT PROTEINS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; OPERON; PLANKTON; RNA, MESSENGER; SEQUENCE DELETION; TOBRAMYCIN;

EID: 84912076708     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.03800-14     Document Type: Article

References (25)

1. Mahenthiralingam E, Urban TA, Goldberg JB. 2005. The multifarious, multireplicon Burkholderia cepacia complex. Nat. Rev. Microbiol. 3:144-156. http://dx.doi.org/10.1038/nrmicro1085.
2. LiPuma JJ. 2010. The changing microbial epidemiology in cystic fibrosis. Clin. Microbiol. Rev. 23:299-323. http://dx.doi.org/10.1128/CMR.00068-09.
3. Peeters E, Nelis HJ, Coenye T. 2008. Evaluation of the efficacy of disinfection procedures against Burkholderia cenocepacia biofilms. J. Hosp. Infect. 70:361-368. http://dx.doi.org/10.1016/j.jhin.2008.08.015.
4. Drevinek P, Mahenthiralingam E. 2010. Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin. Microbiol. Infect. 16:821-830. http://dx.doi.org/10.1111/j.1469-0691.2010 .03237.x.
5. Coenye T. 2010. Social interactions in the Burkholderia cepacia complex: biofilms and quorum sensing. Future Microbiol. 5:1087-1099. http://dx .doi.org/10.2217/fmb.10.68.
6. Van Acker H, Van Dijck P, Coenye T. 2014. Molecular mechanisms of antimicrobial toleranceandresistance in bacterialandfungal biofilms. Trends Microbiol. 22:326-333. http://dx.doi.org/10.1016/j.tim.2014.02.001.
7. Guglierame P, Pasca MR, De Rossi E, Buroni S, Arrigo P, Manina G, Riccardi G. 2006. Efflux pump genes of the resistance-nodulationdivision family in Burkholderia cenocepacia genome. BMC Microbiol. 6:66. http://dx.doi.org/10.1186/1471-2180-6-66.
8. Buroni S, Pasca MR, Flannagan RS, Bazzini S, Milano A, Bertani I, Venturi V, Valvano MA, Riccardi G. 2009. Assessment of three resis-tance-nodulation-cell division drug efflux transporters of Burkholderia cenocepacia in intrinsic antibiotic resistance. BMC Microbiol. 9:200. http: //dx.doi.org/10.1186/1471-2180-9-200.
9. Bazzini S, Udine C, Sass A, Pasca MR, Longo F, Emiliani G, Fondi M, Perrin E, Decorosi F, Viti C, Giovannetti L, Leoni L, Fani R, Riccardi G, Mahenthiralingam E, Buroni S. 2011. Deciphering the role of RND efflux transporters in Burkholderia cenocepacia. PLoS One 6:e18902. http: //dx.doi.org/10.1371/journal.pone.0018902.
10. Perrin E, Fondi M, Papaleo MC, Maida I, Emiliani G, Buroni S, Pasca MR, Riccardi G, Fani R. 2013. A census of RND superfamily proteins in the Burkholderia genus. Future Microbiol. 8:923-937. http://dx.doi.org /10.2217/fmb.13.50.
11. Scoffone VC, Spadaro F, Udine C, Makarov V, Fondi M, Fani R, De Rossi E, Riccardi G, Buroni S. 2014. Mechanism of resistance to an antitubercular 2-thiopyridine derivative that is also active against Burkholderia cenocepacia. Antimicrob. Agents Chemother. 58:2415-2417. http: //dx.doi.org/10.1128/AAC.02438-13.
12. Coenye T, Van Acker H, Peeters E, Sass A, Buroni S, Riccardi G, Mahenthiralingam E. 2011. Molecular mechanisms of chlorhexidine tolerance in Burkholderia cenocepacia biofilms. Antimicrob. Agents Chemother. 55:1912-1919. http://dx.doi.org/10.1128/AAC.01571-10.
13. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
14. 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. http://dx.doi.org/10.1111/j.1462-2920.2008.01576.x.
15. Hamad MA, Skeldon AM, Valvano MA. 2010. Construction of amin-oglycoside-sensitive Burkholderia cenocepacia strains for use in studies of intracellular bacteria with the gentamicin protection assay. Appl. Environ. Microbiol. 76:3170-3176. http://dx.doi.org/10.1128/AEM.03024-09.
16. Craig FF, Coote JG, Parton R, Freer JH, Gilmour NJ. 1989. A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J. Gen. Microbiol. 135:2885-2890.
17. Peeters E, Nelis HJ, Coenye T. 2009. In vitro activity of ceftazidime, ciprofloxacin, meropenem, minocycline, tobramycin and trimethoprim/ sulfamethoxazole against planktonic and sessile Burkholderia cepacia complex bacteria. J. Antimicrob. Chemother. 64:801-809. http://dx.doi .org/10.1093/jac/dkp253.
18. Van Acker H, Sass A, Bazzini S, De Roy K, Udine C, Messiaen T, Riccardi G, Boon N, Nelis HJ, Mahenthiralingam E, Coenye T. 2013. Biofilm-grown Burkholderia cepacia complex cells survive antibiotic treatment by avoiding production of reactive oxygen species. PLoS One 8:e58943. http://dx.doi.org/10.1371/journal.pone.0058943.
19. Van Acker H, Sass A, Dhondt I, Nelis HJ, Coenye T. 2014. Involvement of toxin-antitoxin modules in Burkholderia cenocepacia biofilm persistence. Pathog. Dis. 71:326-335. http://dx.doi.org/10.1111/2049-632X.12177.
20. Peeters E, Nelis H, Coenye T. 2008. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J. Microbiol. Methods 72:157-165. http://dx.doi.org/10.1016/j.mimet.2007.11.010.
21. Kvist M, Hancock V, Klemm P. 2008. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl. Environ. Microbiol. 74:7376-7782. http://dx.doi.org/10.1128/AEM.01310-08.
22. Baugh S, Phillips CR, Ekanayaka AS, Piddock LJ, Webber MA. 2014. Inhibition of multidrug efflux as a strategy to prevent biofilm formation. J. Antimicrob. Chemother. 69:673-681. http://dx.doi.org/10.1093/jac/dkt420.
23. Matsumura K, Furukawa S, Ogihara H, Morinaga Y. 2011. Roles of multidrug efflux pumps on the biofilm formation of Escherichia coli K-12. Biocontrol Sci. 16:69-72. http://dx.doi.org/10.4265/bio.16.69.
24. Miller VL, Mekalanos JJ. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
25. Figurski DH, Helinski DR. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U. S. A. 76:1648-1652. http://dx.doi.org/10 .1073/pnas.76.4.1648.