Growth inhibition of adherent Pseudomonas aeruginosa by an N-butanoyl-L-homoserine lactone analog

Canadian Journal of Microbiology

Volumn 56, Issue 4, 2010, Pages 317-325

  Khalilzadeh, Pouneh ^a   Lajoie, Barbora ^a   El Hage, Salomé ^a   Furiga, Aurélie L ^a   Baziard, Geneviève ^a   Berge, Mathieu ^a   Roques, Christine ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

4 bromo 5 (bromomethylene) 2 (5H) furanone; N acyl homoserine lactone (AHL); Pseudomonas aeruginosa; Quorum sensing

Indexed keywords

ADHERENT CELLS; AUTOINDUCERS; BIOFILM FORMATION; BIOLOGICAL ACTIVITIES; DOSE-DEPENDENT MANNER; FURANONES; GROWTH INHIBITION; HOMOSERINE LACTONES; HUMAN PATHOGENS; LACTONE MOIETY; N-ACYL HOMOSERINE LACTONES; POTENT INHIBITOR; PSEUDOMONAS AERUGINOSA; QUORUM-SENSING; RELATED COMPOUNDS; STRUCTURE ACTIVITY RELATIONSHIPS; VIRULENCE FACTORS;

AMINO ACIDS; BACTERIOLOGY; BIOACTIVITY; BIOFILMS; BIOFILTERS; COMMUNICATION SYSTEMS; GROWTH KINETICS;

BACTERIA;

ANTIBIOTIC AGENT; LACTONE DERIVATIVE; N BUTANOYL LEVO HOMOSERINE LACTONE; UNCLASSIFIED DRUG;

ANTAGONISM; BACTERIUM; BIOCHEMICAL COMPOSITION; BIOCHEMISTRY; BIOFILM; MICROBIAL ACTIVITY; PATHOGENICITY; VIRULENCE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; BIOFILM; CELL ADHESION; CONTROLLED STUDY; DRUG SCREENING; GROWTH INHIBITION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; STRUCTURE ACTIVITY RELATION;

4-BUTYROLACTONE; ANTI-BACTERIAL AGENTS; BIOFILMS; DRUG DESIGN; DRUG EVALUATION, PRECLINICAL; HUMANS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; QUORUM SENSING; STRUCTURE-ACTIVITY RELATIONSHIP; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 77951657307     PISSN: 00084166     EISSN: None     Source Type: Journal    
DOI: 10.1139/W10-013     Document Type: Article

References (39)

1. Bottomley, M.J., Muraglia, E., Bazzo, R., and Carfì. A. 2007. Molecular insights into quorum sensing in the human pathogen Pseudomonas aeruginosa from the structure of the virulence regulator LasR bound to its autoinducer. J. Biol. Chem. 282(18): 13592-13600. doi:10.1074/jbc.M700556200. PMID: 17363368.
2. Campanac, C., Pineau, L., Payard, A., Baziard-Mouysset, G., and Roques, C. 2002. Interactions between biocide cationic agents and bacterial biofilms. Antimicrob. Agents Chemother. 46(5): 1469-1474. doi:10.1128/AAC.46.5.1469-1474. 2002. PMID: 11959584.
3. Costerton, J.W., Stewart, P.S., and Greenberg, E.P. 1999. Bacterial biofilms: a common cause of persistent infections. Science (Washington, D.C.), 284(5418): 1318-1322. doi:10.1126/science. 284.5418.1318. PMID:10334980. (Pubitemid 29289651)
4. Davies, D.G., Parsek, M.R., Pearson, J.P., Iglewski, B.H., Costerton, J.W., and Greenberg, E.P. 1998. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science (Washington, D.C.), 280(5361): 295-298. doi:10.1126/science. 280.5361.295. PMID:9535661.
5. de Kievit, T.R., and Iglewski, B.H. 2000. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68(9): 4839-4849. doi:10.1128/IAI.68.9. 4839-4849.2000. PMID:10948095.
6. de Kievit, T.R., Gillis, R., Marx, S., Brown, C., and Iglewski, B.H. 2001. Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl. Environ. Microbiol. 67(4): 1865-1873. doi:10.1128/AEM.67.4.1865-1873.2001. PMID:11282644.
7. Dong, W., Luo, F., Du, Y., Bai, X., and Li, X. 2005. Production and properties of an inhibitor of the Pseudomonas autoinducer by Pseudomonas aeruginosa. Can. J. Microbiol. 51(9): 783-789. doi:10.1139/w05-066. PMID:16391658.
8. Duan, K., and Surette, M.G. 2007. Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J. Bacteriol. 189(13): 4827-4836. doi:10.1128/JB. 00043-07. PMID:17449617.
9. Favre-Bonté, S., Pache, J.C., Robert, J., Blanc, D., Pechère, J.C., and van Delden, C. 2002. Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients. Microb. Pathog. 32(3): 143-147. doi:10.1006/mpat.2001.0487. PMID:11855945.
10. Fuqua, C., and Greenberg, E.P. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3(9): 685-695. doi:10.1038/nrm907. PMID:12209128.
11. Geske, G.D., Wezeman, R.J., Siegel, A.P., and Blackwell, H.E. 2005. Small molecule inhibitors of bacterial quorum sensing and biofilm formation. J. Am. Chem. Soc. 127(37): 12762-12763. doi:10.1021/ja0530321. PMID:16159245.
12. Hall-Stoodley, L., Costerton, J.W., and Stoodley, P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2(2): 95-108. doi:10.1038/nrmicro821. PMID:15040259.
13. Hayes, D., Jr., Kanga, J.F., Anstead, M.I., and Kuhn, R.J. 2008. Novel approach to the eradication of Pseudomonas aeruginosa in an infant with CF after outpatient treatment failure. Pediatr. Pulmonol. 43(5): 511-513. doi:10.1002/ppul.20791. PMID: 18383117.
14. Høiby, N.B., Krogh Johansen, H., Moser, C., Song, Z., Ciofu, O., and Kharazmi, A. 2001. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect. 3(1): 23-35. doi:10.1016/S1286-4579(00) 01349-6. PMID:11226851.
15. Huang, J.J., Petersen, A., Whiteley, M., and Leadbetter, J.R. 2006. Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 72(2): 1190-1197. doi:10.1128/AEM.72.2.1190-1197.2006. PMID:16461666.
16. Juhas, M., Eberl, L., and Tümmler, B. 2005. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ. Microbiol. 7(4): 459-471. doi:10.1111/j.1462-2920.2005.00769. x. PMID:15816912. (Pubitemid 40441020)
17. Kim, C., Kim, J., Park, H.-Y., Park, H.-J., Lee, J.H., Kim, C.K., and Yoon, J. 2008. Furanone derivatives as quorum-sensing antagonists of Pseudomonas aeruginosa. Appl. Microbiol. Biotechnol. 80(1): 37-47. doi:10.1007/s00253-008- 1474-6. PMID: 18566810.
18. Manny, A.J., Kjelleberg, S., Kumar, N., de Nys, R., Read, R.W., and Steinberg, P. 1997. Reinvestigation of the sulfuric acid-catalysed cyclisation of brominated 2-alkyllevulinic acids to 3-alkyl-5-methylene-2-(5H)-furanones. Tetrahedron, 53(46): 15813-15826. doi:10.1016/S0040-4020(97)10034-5.
19. Martinelli, D., Grossmann, G., Séquin, U., Brandl, H., and Bachofen, R. 2004. Effects of natural and chemically synthesized furanones on quorum sensing in Chromobacterium violaceum. BMC Microbiol. 4(1): 25. doi:10.1186/1471-2180-4-25. PMID: 15233843.
20. McLean, R.J., Pierson, L.S., 3rd, and Fuqua, C. 2004. A simple screening protocol for the identification of quorum signal antagonists. J. Microbiol. Methods, 58(3): 351-360. doi:10.1016/j. mimet.2004.04.016. PMID:15279939.
21. Middleton, B., Rodgers, H.C., Cámara, M., Knox, A.J., Williams, P., and Hardman, A. 2002. Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol. Lett. 207(1): 1-7. doi:10.1111/j.1574- 6968.2002.tb11019.x. PMID: 11886742.
22. O'May, C.Y., Reid, D.W., and Kirov, S.M. 2006. Anaerobic culture conditions favor biofilm-like phenotypes in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. FEMS Immunol. Med. Microbiol. 48(3): 373-380. doi:10.1111/j.1574-695X.2006.00157.x. PMID:17052266.
23. Olsen, J.A., Severinsen, R., Rasmussen, T.B., Hentzer, M., Givskov, M., and Nielsen, J. 2002. Synthesis of new 3- and 4-substituted analogues of acyl homoserine lactone quorum sensing autoinducers. Bioorg. Med. Chem. Lett. 12(3): 325-328. doi:10. 1016/S0960-894X(01)00756-9. PMID:11814788.
24. Park, S.Y., Kang, H.O., Jang, H.S., Lee, J.K., Koo, B.T., and Yum, D.Y. 2005. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 71(5): 2632-2641. doi:10.1128/AEM.71.5.2632-2641.2005. PMID:15870355.
25. Parsek, M.R., and Greenberg, E.P. 2000. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. U.S.A. 97(16): 8789-8793. doi:10.1073/pnas.97.16. 8789. PMID:10922036.
26. Pearson, J.P., Feldman, M., Iglewski, B.H., and Prince, A. 2000. Pseudomonas aeruginosa cell-to-cell signaling is required for virulence in a model of acute pulmonary infection. Infect. Immun. 68(7): 4331-4334. doi:10.1128/IAI.68.7.4331-4334.2000. PMID:10858254.
27. Pedretti, A., Villa, L., and Vistoli, G. 2002. VEGA: a versatile program to convert, handle and visualize molecular structure on Windows-based PCs. J. Mol. Graph. Model. 21(1): 47-49. doi:10.1016/S1093-3263(02)00123-7. PMID:12413030.
28. Rasmussen, T.B., and Givskov, M. 2006. Quorum sensing inhibitors: a bargain of effects. Microbiology, 152(4): 895-904. doi:10.1099/mic.0.28601-0. PMID:16549654.
29. Reverchon, S., Chantegrel, B., Deshayes, C., Doutheau, A., and Cotte-Pattat, N. 2002. New synthetic analogues of N-acyl homoserine lactones as agonists or antagonists of transcriptional regulators involved in bacterial quorum sensing. Bioorg. Med. Chem. Lett. 12(8): 1153-1157. doi:10.1016/S0960- 894X(02) 00124-5. PMID:11934577.
30. Robson, N.D., Cox, A.R., McGowan, S.J., Bycroft, B.W., and Salmond, G.P. 1997. Bacterial N-acyl-homoserine-lactonedependent signalling and its potential biotechnological applications. Trends Biotechnol. 15(11): 458-464. doi:10.1016/S0167-7799(97)01102-5. PMID:9369029.
31. Ruimy, R., and Andremont, A. 2004. Quorum sensing in Pseudomonas aeruginosa: molecular mechanism, clinical impact and inhibition. Reanimation, 13: 176-184. doi:10.1016/j.reaurg. 2004.02.003.
32. Smith, K.M., Bu, Y., and Suga, H. 2003. Library screening for synthetic agonists and antagonists of a Pseudomonas aeruginosa autoinducer. Chem. Biol. 10(6): 563-571. doi:10.1016/S1074-5521(03)00107-8. PMID:12837389.
33. Soulère, L., Guiliani, N., Queneau, Y., Jerez, C.A., and Doutheau, A. 2008. Molecular insights into quorum sensing in Acidithiobacillus ferrooxidans bacteria via molecular modelling of the transcriptional regulator AfeR and of the binding mode of longchain acyl homoserine lactones. J. Mol. Model. 14(7): 599-606. doi:10.1007/s00894-008-0315-y. PMID:18478280.
34. Stewart, J.J.P. 2007. Optimization of parameters for semiempirical methods V: modification of NDDO approximations and application to 70 elements. J. Mol. Model. 13(12): 1173-1213. doi:10. 1007/s00894-007-0233-4. PMID:17828561.
35. Stewart, J.J.P. 2009. Stewart Computational Chemistry, Colorado Springs, CO, USA, MOPAC2009.
36. Van Delden, C., and Iglewski, B.H. 1998. Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 4(4): 551-560. doi:10.3201/eid0404.980405. PMID:9866731.
37. Williams, P., Camara, M., Hardman, A., Swift, S., Milton, D., Hope, V.J., et al. 2000. Quorum sensing and the populationdependent control of virulence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355(1397): 667-680. doi:10.1098/rstb.2000.0607. PMID:10874739.
38. Wood, D.M., and Smyth, A. 2006. Antibiotic strategies for eradicating Pseudomonas aeruginosa in people with cystic fibrosis. Cochrane Database Syst. Rev. 25(1): CD004197.
39. Wu, H., Song, Z., Hentzer, M., Andersen, J.B., Molin, S., Givskov, M., and Høiby, N. 2004. Synthetic furanones inhibit quorumsensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J. Antimicrob. Chemother. 53(6): 1054-1061. doi:10.1093/jac/dkh223. PMID:15117922.