A quorum sensing-disrupting brominated thiophenone with a promising therapeutic potential to treat luminescent vibriosis

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Defoirdt, Tom ^a   Benneche, Tore ^b   Brackman, Gilles ^a   Coenye, Tom ^a   Sorgeloos, Patrick ^a   Scheie, Anne Aamdal ^b  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

4 [[5 (BROMOMETHYLENE) 2 OXO 2,5 DIHYDROTHIOPHEN 3 YL]METHOXY] 4 OXOBUTANOIC ACID; 5 (BROMOMETHYLENE)THIOPHEN 2(5H) ONE; BACTERIAL DNA; TF 101; TF 310; THIOPHENE DERIVATIVE; TRANSCRIPTION FACTOR LUXR; UNCLASSIFIED DRUG;

ARTEMIA; ARTICLE; BIOLUMINESCENCE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFICACY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; GNOTOBIOTICS; IN VIVO STUDY; NONHUMAN; PROTEIN DNA BINDING; QUORUM SENSING; TREATMENT RESPONSE; VIBRIO HARVEYI; VIBRIOSIS;

ANIMALS; ARTEMIA; DNA, BACTERIAL; LARVA; LUMINESCENT MEASUREMENTS; MUTATION; PROMOTER REGIONS, GENETIC; QUORUM SENSING; REPRESSOR PROTEINS; SUCCINATES; THIOPHENES; TRANS-ACTIVATORS; VIBRIO; VIBRIO INFECTIONS;

ARTEMIA; BACTERIA (MICROORGANISMS); VIBRIO HARVEYI;

EID: 84864663142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041788     Document Type: Article

References (38)

1. Austin B, Zhang X-H, (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43: 119-124.
2. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P, (2007) Alternatives to antibiotics to control bacterial infections- luminescent vibriosis in aquaculture as an example. Trends Biotechnol 25: 472-479.
3. Waters CM, Bassler BL, (2006) The Vibrio harveyi quorum-sensing system used shared regulatory components to discriminate between multiple autoinducers. Genes Dev 20: 2754-2767.
4. Henke JM, Bassler BL, (2004) Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186: 3794-3805.
5. Manefield M, Harris L, Rice SA, de Nys R, Kjelleberg S, (2000) Inhibition of luminescence and virulence in the black tiger prawn (Penaeus monodon) pathogen Vibrio harveyi by intercellular signal antagonists. Appl Environ Microbiol 66: 2079-2084.
6. Mok KC, Wingreen NS, Bassler BL, (2003) Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22: 870-881.
7. Lilley BN, Bassler BL, (2000) Regulation of quorum sensing in Vibrio harveyi by LuxO and σ54. Mol Microbiol 36: 940-954.
8. Defoirdt T, Ruwandeepika HAD, Karunasagar I, Boon N, Bossier P, (2010) Quorum sensing negatively regulates chitinase in Vibrio harveyi. Environ Microbiol Rep 2: 44-49.
9. Natrah FMI, Ruwandeepika HAD, Pawar S, Karunasagar I, Sorgeloos P, et al. (2011) Regulation of virulence factors by quorum sensing in Vibrio harveyi. Vet Microbiol 154: 124-129.
10. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P, (2008) Quorum sensing and quorum quenching in Vibrio harveyi: lessons learned from in vivo work. ISME J 2: 19-26.
11. Rasmussen TB, Givskov M, (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296: 149-161.
12. Janssens JCA, De Keersmaecker SCJ, De Vos DE, Vanderleyden J, (2008) Small molecules for interference with cell-cell-communication systems in Gram-negative bacteria. Curr Med Chem 15: 2144-2156.
13. Pan J, Ren D, (2009) Quorum sensing inhibitors: a patent overview. Expert Opin Ther Patents 19: 1581-1601.
14. Defoirdt T, Miyamoto C, Wood TK, Meighen EA, Sorgeloos P, et al. (2007) The natural furanone (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone disrupts quorum sensing-regulated gene expression in Vibrio harveyi by decreasing the DNA-binding activity of the transcriptional regulator protein luxR. Environ Microbiol 9: 2486-2495.
15. Rasch M, Buch C, Austin B, Slierendrecht WJ, Ekmann KS, et al. (2004) An inhibitor of bacterial quorum sensing reduces mortalities caused by vibriosis in rainbow trout (Oncorhynchus mykiss, Walbaum). System Appl Microbiol 27: 350-359.
16. Defoirdt T, Crab R, Wood TK, Sorgeloos P, Verstraete W, et al. (2006) Quorum sensing-disrupting brominated furanones protect the gnotobiotic brine shrimp Artemia franciscana from pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus isolates. Appl Environ Microbiol 72: 6419-6423.
17. Tinh NTN, Linh ND, Wood TK, Dierckens K, Sorgeloos P, et al. (2007) Interference with the quorum sensing systems in a Vibrio harveyi strain alters the growth rate of gnotobiotically cultured rotifer Brachionus plicatilis. J Appl Microbiol 103: 194-203.
18. Benneche T, Herstad G, Rosenberg ML, Assev S, Scheie AA, (2011) Facile synthesis of 5-(alkylidene)thiophen-2(5H)-ones. A new class of antimicrobial agents. RSC Advances 1: 323-332.
19. Lönn-Stensrud J, Benneche T, Scheie AA, (2011) Furanones and thiophenones in control of Staphylococcus epidermidis biofilm infections? In: Mendez-Vilas A, editors. Science and Technology against Microbial Pathogens. Research, Development and Evaluation pp. 155-159 In: World Scientific Publishing Co.
20. Lönn-Stensrud J, Naemi A, Benneche T, Scheie AA, (2012) Thiophenones inhibit Staphylococcus epidermidis biofilm formation at non-toxic concentrations. FEMS Immunol Med Microbiol 65: 326-34.
21. Henke JM, Bassler BL, (2004) Three parallel quorum sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186: 6902-6914.
22. Freeman JA, Bassler BL, (1999) A genetic analysis of the function of LuxO, a two-component response regulator involved in quorum sensing in Vibrio harveyi. Mol Microbiol 31: 665-677.
23. Freeman JA, Bassler BL, (1999) Sequence and function of LuxU: a two-component phosphorelay protein that regulates quorum sensing in Vibrio harveyi. J Bacteriol 181: 899-906.
24. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, et al. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118: 69-82.
25. Karsi A, Menanteau-Ledouble S, Lawrence ML, (2006) Development of bioluminescent Edwardsiella ictulari for noninvasive disease monitoring. FEMS Microbiol Lett 260: 216-223.
26. Zang T, Lee BWK, Cannon LM, Ritter KA, Dai S, et al. (2009) A naturally occurring brominated furanone covalently modifies and inactivates LuxS. Bioorg Med Chem Lett 19: 6200-6204.
27. Benneche T, Chamgordani EJ, Scheie AA, (2012) Reaction of (Z)-5-bromomethylene)thiophen-2(5H)-one with some nucleophiles in search for new biofilm inhibitors. Synth Commun in press.
28. De Silva RS, Kovacikova G, Lin W, Taylor RK, Skorupski K, et al. (2007) Crystal structure of the Vibrio cholerae quorum-sensing regulatory protein HapR. J Bacteriol 189: 5683-5691.
29. Ramos JL, Martínez-Bueno M, Molina-Henares AJ, Terán W, Watanabe K, et al. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356.
30. Janssens JCA, Steenackers H, Robijns S, Gellens E, Levin J, et al. (2008) Brominated furanones inhibit biofilm formation by Salmonella enterica serovar Typhimurium. Appl Environ Microbiol 74: 6639-6648.
31. Steenackers HP, Levin J, Janssens JC, De Weerdt A, Balzarini J, et al. (2010) Structure-activity relationship of brominated 3-alkyl-5-methylene-2(5H)-furanones and alkylmaleic anhydrides as inhibitors of Salmonella biofilm formation and quorum sensing regulated bioluminescence in Vibrio harveyi. Bioorg Med Chem 18: 5224-5233.
32. Brackman G, Defoirdt T, Miyamoto CM, Bossier P, Van Calenbergh S, et al. (2008) Cinnamaldehyde and cinnamaldehyde derivatives reduce virulence in Vibrio spp. by decreasing the DNA-binding activity of the quorum sensing response regulator LuxR. BMC Microbiol 8: 149.
33. Brackman G, Celen S, Baruah K, Bossier P, Van Calenbergh S, et al. (2009) AI-2 quorum-sensing inhibitors affect the starvation response and reduce virulence in several Vibrio species, most likely by interfering with LuxPQ. Microbiology 155: 4114-4122.
34. Benneche T, Hussain Z, Scheie AA, Lönn-Stensrud J, (2008) Synthesis of 5-(bromo-methylene)furan-2(5H)-ones and 3-(bromomethylene)isobenzofuran-1(3H)-ones as inhibitors of microbial quorum sensing. New J Chem 32: 1567-1572.
35. Bassler BL, Greenberg EP, Stevens AM, (1997) Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J Bacteriol 179: 4043-4045.
36. Pompeani AJ, Irgon JJ, Berger MF, Bulyk ML, Wingreen NS, et al. (2008) The Vibrio harveyi master quorum-sensing regulator, LuxR, a TetR-type protein is both an activator and a repressor: DNA recognition and binding specificity at target promoters. Mol Microbiol 70: 76-88.
37. Brackman G, Celen S, Hillaert U, Van Calenbergh S, Cos P, et al. (2011) Structure-activity relationship of cinnamaldehyde analogs as inhibitors of AI-2 based quorum sensing and their effect on virulence of Vibrio spp. PLoS ONE 6: e16084.
38. Defoirdt T, Bossier P, Sorgeloos P, Verstraete W, (2005) The impact of mutations in the quorum sensing systems of Aeromonas hydrophila, Vibrio anguillarum and Vibrio harveyi on their virulence towards gnotobiotically cultured Artemia franciscana. Environ Microbiol 7: 1239-1247.