Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 6, 2011, Pages 2655-2661

  Brackman, Gilles ^a   Cos, Paul ^b   Maes, Louis ^b   Nelis, Hans J ^a   Coenye, Tom ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BAICALIN; CINNAMALDEHYDE; CLINDAMYCIN; HAMAMELITANNIN; N ACYLHOMOSERINE LACTONE; QUORUM SENSING INHIBITOR; TOBRAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC SENSITIVITY; ANTIBIOTIC THERAPY; ARTICLE; BACTERICIDAL ACTIVITY; BIOFILM; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DRUG EFFECT; FEMALE; GALLERIA MELLONELLA; LARVA; LUNG INFECTION; MOUSE; NONHUMAN; PARASITE SURVIVAL; PATHOGEN LOAD; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BIOFILMS; FEMALE; FLAVONOIDS; MICE; MICE, INBRED BALB C; MICROBIAL SENSITIVITY TESTS; QUORUM SENSING; TOBRAMYCIN;

EID: 79956311555     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00045-11     Document Type: Article

References (45)

1. Begun, J., et al. 2007. Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog. 3:e57.
2. Blom, D., C. Fabbri, L. Eberl, and L. Weisskopf. 2011. Volatile-mediated killing of Arabidopsis thaliana by bacteria is mainly due to hydrogen cyanide. Appl. Environ. Microbiol. 77:1000-1008.
3. Boles, B. R., and A. R. Horswill. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4:e1000052.
4. Brackman, G., U. Hillaert, S. Van Calenbergh, H. J. Nelis, and T. Coenye. 2009. Use of quorum sensing inhibitors to interfere with biofilm formation and development in Burkholderia multivorans and Burkholderia cenocepacia. Res. Microbiol. 160:144-151.
5. Cooper, V. S., W. A. Carlson, and J. J. LiPuma. 2009. Susceptibility of Caenorhabditis elegans to Burkholderia infection depends on prior diet and secreted bacterial attractants. PLoS One 4:e7961.
6. Dhakal, B. K., et al. 2006. Caenorhabditis elegans as a simple model host for Vibrio vulnificus infection. Biochem. Biophys. Res. Commun. 346:751-757.
7. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
8. Elborn, J. S., M. Hodson, and C. Bertram. 2009. Implementation of European standards of care for cystic fibrosis-control and treatment of infection. J. Cyst. Fibrosis 8:211-217.
9. Estrela, A. B., M. G. Heck, and W. R. Abraham. 2009. Novel approaches to control biofilm infections. Curr. Med. Chem. 16:1512-1530.
10. Fuqua, C., and E. P. Greenberg. 2002. Listening in on bacteria: acyl-homoserine lactone signaling. Nat. Rev. Mol. Cell. Biol. 3:685-695.
11. Gao, W., et al. 2010. Two novel point mutations in clinical Staphylococcus aureus reduce linezolid susceptibility and switch on the stringent response to promote persistent infection. PLoS Pathog. 6:e1000944.
12. Gemmell, C. G., et al. 2006. Guidelines for the prophylaxis and treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections in the UK. J. Antimicrob. Chemother. 57:589-608.
13. George, A. M., P. M. Jones, and P. G. Middleton. 2009. Cystic fibrosis infections: treatment strategies and prospects. FEMS Microbiol. Lett. 300:153-164.
14. Hall-Stoodley, L., J. W. Costerton, and P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2:95-108.
15. Hardie, K. R., and K. Heurlier. 2008. Establishing bacterial communities by 'word of mouth': LuxS and autoinducer 2 in biofilm development. Nat. Rev. Microbiol. 6:635-643.
16. Henry, D., et al. 1999. Comparison of isolation media for the recovery of Burkholderia cepacia complex from respiratory secretions of patients with cystic fibrosis. J. Clin. Microbiol. 37:1004-1007.
17. Høiby, N., T. Bjarnsholt, M. Givskov, S. Molin, and O. Ciofu. 2010. Antibiotic resistance of bacterial biofilms. Int. J. Antimicrob. Agents 35:322-332.
18. Huber, B., et al. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517-2528. (Pubitemid 32899247)
19. Huber, B., et al. 2004. Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect. Immun. 72:7220-7230.
20. Irie, Y., and M. R. Parsek. 2008. Quorum sensing and microbial biofilms. Curr. Top. Microbiol. Immunol. 322:67-84.
21. Kiran, M. D., et al. 2008. Discovery of a quorum sensing inhibitor of drug-resistant staphylococcal infections by structure-based virtual screening. Mol. Pharmacol. 73:1578-1586.
22. Kong, K. F., C. Vuong, and M. Otto. 2006. Staphylococcus quorum sensing in biofilm formation and infection. Int. J. Med. Microbiol. 296:133-139.
23. Lipsky, B. A., and C. Hoey. 2009. Topical antimicrobial therapy for treating chronic wounds. Clin. Infect. Dis. 49:1541-1549.
24. Macedo, A. J., and W. R. Abraham. 2009. Can. infectious biofilm be controlled by blocking bacterial communication? Med. Chem. 5:517-528.
25. Martin, J. M., J. M. Zenilman, and G. S. Lazarus. 2010. Molecular microbiology: new dimensions for cutaneous biology and wound healing. J. Invest. Dermatol. 130:38-48.
26. Miller, M. B., and B. L. Bassler. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165-199.
27. Moy, T. I., et al. 2009. High-throughput screen for novel antimicrobial using a whole animal infection model. ACS Chem. Biol. 4:527-533.
28. Musk, D. J., Jr., and P. J. Hergenrother. 2006. Chemical countermeasures for the control of bacterial biofilms: effective compounds and promising targets. Curr. Med. Chem. 13:2163-2177.
29. Palmer, K. L., L. M. Aye, and M. Whiteley. 2007. Nutritional cues control Pseudomonas aeruginosa multicellular behavior in cystic fibrosis sputum. J. Bacteriol. 189:8079-8087. (Pubitemid 350178919)
30. Parsek, M. R., and P. K. Singh. 2003. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57:677-701.
31. Peeters, E., H. J. Nelis, and T. Coenye. 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.
32. Rau, M. H., et al. 2010. Early adaptive developments of Pseudomonas aeruginosa after the transition from life in the environment to persistent colonization in the airways of human cystic fibrosis hosts. Environ. Microbiol. 12:1643-1658.
33. Sifri, C. D., J. Begun, F. M. Ausubel, and S. B. Calderwood. 2003. Caenorhabditis elegans as a model for Staphylococcal aureus pathogenesis. Infect. Immun. 71:2208-2217.
34. Sopirala, M. M., et al. 2010. Synergy testing by Etest, microdilution checkerboard, and time-kill methods for pan-drug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 54:4678-4683.
35. Sriramulu, D. D., H. Lünsdorf, J. S. Lam, and U. Römling. 2005. Microcolony formation: a novel biofilm model of Pseudomonas aeruginosa for the cystic fibrosis lung. J. Med. Microbiol. 54:667-676.
36. Stiernagle, T. 2006. Maintenance of C. elegans. Wormbook 11:1-11.
37. Sun, Y., S. E. Dowd, E. Smith, D. D. Rhoads, and R. D. Wolcott. 2008. In vitro multispecies Lubbock chronic wound biofilm model. Wound Repair Regen. 16:805-813.
38. Sutherland, I. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147:3-9. (Pubitemid 32094304)
39. Tomlin, K. L., et al. 2005. Quorum-sensing mutations affect attachment and stability of Burkholderia cenocepacia biofilms. Appl. Environ. Microbiol. 71:5208-5218.
40. Uehlinger, S., et al. 2009. Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect. Immun. 77:4102-4110.
41. Werthén, M., et al. 2010. An in vitro model of bacterial infections in wounds and other soft tissues. APMIS 118:156-164.
42. Williams, P. 2007. Quorum sensing, communication and cross-kingdom signaling in the bacterial world. Microbiology 153:3923-3938.
43. Xavier, K. B., and B. L. Bassler. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191-197.
44. Yang, L., et al. 2009. Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum sensing inhibitors. Antimicrob. Agents Chemother. 53:2432-2443.
45. Zeng, L., et al. 2008. Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 79:119-126.