Suppression of bacterial cell-cell signalling, biofilm formation and type III secretion system by citrus flavonoids

Journal of Applied Microbiology

Volumn 109, Issue 2, 2010, Pages 515-527

  Vikram, A ^a   Jayaprakasha, G K ^a   Jesudhasan, P R ^a   Pillai, S D ^a   Patil, B S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

EHEC; flavonoids; naringenin; quorum sensing; real time PCR; TTSS

Indexed keywords

ASSAYS; BIOFILMS; CELL SIGNALING; CYTOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; LEAD COMPOUNDS; METABOLITES; PHENOLS; PHYSIOLOGY; PLANTS (BOTANY); POLYMERASE CHAIN REACTION;

APIGENIN; BACTERIAL CELLS; BIOFILM FORMATION; CELL-CELL SIGNALING; EHEC; FLAVONOID; NARINGENIN; QUORUM-SENSING; REAL-TIME PCR; TYPE THREE SECRETION SYSTEMS;

FLAVONOIDS;

APIGENIN; BIOFLAVONOID; HESPERIDIN; KAEMPFEROL; NARINGENIN; NEOERIOCITRIN; NEOHESPERIDIN; QUERCETIN; RUTOSIDE; SINENSETIN; UNCLASSIFIED DRUG;

BACTERIUM; BIOFILM; COLIFORM BACTERIUM; EXPERIMENTAL STUDY; GENE EXPRESSION; POLYMERASE CHAIN REACTION; REAL TIME; SECRETION;

ARTICLE; BACTERIAL CELL; BIOFILM; BIOLUMINESCENCE; CELL COMMUNICATION; CELL SECRETION; CHEMICAL STRUCTURE; ESCHERICHIA COLI O157; GENE EXPRESSION; NONHUMAN; POLYMERASE CHAIN REACTION; QUORUM SENSING; TYPE THREE SECRETION SYSTEM; VIBRIO HARVEYI;

BACTERIA (MICROORGANISMS); CITRUS; ESCHERICHIA COLI; VIBRIO HARVEYI;

EID: 77954514638     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2010.04677.x     Document Type: Article

References (59)

1. Adonizio, A.L., Downum, K., Bennett, B.C. Mathee, K. (2006) Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 105, 427 435.
2. Ahmer, B.M.M. (2004) Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 52, 933 945.
3. Basile, A., Giordano, S., Lopez-Saez, J.A. Cobianchi, R.C. (1999) Antibacterial activity of pure flavonoids isolated from mosses. Phytochemistry 52, 1479 1482.
4. Basile, A., Sorbo, S., Giordano, S., Ricciardi, L., Ferrara, S., Montesano, D., Castaldo Cobianchi, R., Vuotto, M.L. et al. (2000) Antibacterial and allelopathic activity of extract from Castanea sativa leaves. Fitoterapia 71, S110 S116.
5. Basile, A., Sorbo, S., Lopez-Saez, J.A. Castaldo Cobianchi, R. (2003) Effects of seven pure flavonoids from mosses on germination and growth of Tortula muralis HEDW. (Bryophyta) and Raphanus sativus L. (Magnoliophyta). Phytochemistry 62, 1145 1151.
6. Bassler, B.L. (2002) Small talk: cell-to-cell communication in bacteria. Cell 109, 421 424.
7. Bassler, B.L. Losick, R. (2006) Bacterially speaking. Cell 125, 237 246.
8. Benavente-Garcia, O. Castillo, J. (2008) Update on uses and properties of citrus flavonoids: new findings in anticancer, cardiovascular, and anti-inflammatory activity. J Agric Food Chem 56, 6185 6205.
9. Benavente-Garcia, O., Castillo, J., Marin, F.R., Ortuno, A. Del Rio, J.A. (1997) Uses and properties of citrus flavonoids. J Agric Food Chem 45, 4505 4515.
10. Borchardt, S.A., Allain, E.J., Michels, J.J., Stearns, G.W., Kelly, R.F. McCoy, W.F. (2001) Reaction of acylated homoserine lactone bacterial signaling molecules with oxidized halogen antimicrobials. Appl Environ Microbiol 67, 3174 3179.
11. Brackman, G., Defoirdt, T., Miyamoto, C., Bossier, P., Van Calenbergh, S., Nelis, H. Coenye, T. (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.
12. Calabro, M.L., Galtieri, V., Cutroneo, P., Tommasini, S., Ficarra, P. Ficarra, R. (2004) Study of the extraction procedure by experimental design and validation of a LC method for determination of flavonoids in Citrus bergamia juice. J Pharm Biomed Anal 35, 349 363.
13. Camilli, A. Bassler, B.L. (2006) Bacterial small-molecule signaling pathways. Science 311, 1113 1116.
14. Castang, S., Chantegrel, B., Deshayes, C., Dolmazon, R., Gouet, P., Haser, R., Reverchon, S., Nasser, W. et al. (2004) N-Sulfonyl homoserine lactones as antagonists of bacterial quorum sensing. Bioorg Med Chem Lett 14, 5145 5149.
15. Choi, J., Shin, D. Ryu, S. (2007) Implication of quorum sensing in Salmonella enterica Serovar Typhimurium virulence: the luxS gene is necessary for expression of genes in pathogenicity island 1. Infect Immun 75, 4885 4890.
16. Choo, J.H., Rukayadi, Y. Hwang, J.K. (2006) Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 42, 637 641.
17. Chorianopoulos, N.G., Giaouris, E.D., Skandamis, P.N., Haroutounian, S.A. Nychas, G.-J.E. (2008) Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. J Appl Microbiol 104, 1586 1596.
18. Costerton, J.W., Stewart, P.S. Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284, 1318 1322.
19. Croxatto, A., Chalker, V.J., Lauritz, J., Jass, J., Hardman, A., Williams, P., Camara, M. Milton, D.L. (2002) VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J Bacteriol 184, 1617 1629.
20. Cushnie, T.P.T. Lamb, A.J. (2005) Antimicrobial activity of flavonoids. Int J Antimicrob Agents 26, 343 356.
21. 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.
22. Defoirdt, T., Crab, R., Wood, T.K., Sorgeloos, P., Verstraete, W. Bossier, P. (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.
23. Defoirdt, T., Miyamoto, C.M., Wood, T.K., Meighen, E.A., Sorgeloos, P., Verstraete, W. Bossier, P. (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.
24. Duarte, S., Gregoire, S., Singh, A.P., Vorsa, N., Schaich, K., Bowen, W.H. Koo, H. (2006) Inhibitory effects of cranberry polyphenols on formation and acidogenicity of Streptococcus mutans biofilms. FEMS Microbiol Lett 257, 50 56.
25. Evans, D.G., Evans, D.J. Jr. Tjoa, W. (1977) Hemagglutination of human Group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor. Infect Immun 18, 330 337.
26. Fotsis, T., Pepper, M.S., Aktas, E., Breit, S., Rasku, S., Adlercreutz, H., Wahala, K., Montesano, R. et al. (1997) Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res 57, 2916 2921.
27. Fuqua, C., Parsek, M.R. Greenberg, E.P. (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35, 439 468.
28. Gatto, M.T., Falcocchio, S., Grippa, E., Mazzanti, G., Battinelli, L., Nicolosi, G., Lambusta, D. Saso, L. (2002) Antimicrobial and anti-lipase activity of quercetin and its C2-C16 3-O-acyl-esters. Bioorg Med Chem 10, 269 272.
29. Gattuso, G., Barreca, D., Gargiulli, C., Leuzzi, U. Caristi, C. (2007) Flavonoid composition of citrus juices. Molecules 12, 1641 1673.
30. Gonzalez Barrios, A.F., Zuo, R., Hashimoto, Y., Yang, L., Bentley, W.E. Wood, T.K. (2006) Autoinducer 2 controls biofilm formation in Escherichia coli through a novel motility quorum-sensing regulator (MqsR, B3022). J Bacteriol 188, 305 316.
31. Hammer, B.K. Bassler, B.L. (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50, 101 104.
32. Heim, K.E., Tagliaferro, A.R. Bobilya, D.J. (2002) Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13, 572 584.
33. Henke, J.M. Bassler, B.L. (2004a) Quorum sensing regulates type III secretion in Vibrio harveyi and Vibrio parahaemolyticus. J Bacteriol 186, 3794 3805.
34. Henke, J.M. Bassler, B.L. (2004b) Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol 186, 6902 6914.
35. Hentzer, M. Givskov, M. (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112, 1300 1307.
36. Jackson, D.W., Suzuki, K., Oakford, L., Simecka, J.W., Hart, M.E. Romeo, T. (2002) Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184, 290 301.
37. Lewis, K. (2001) Riddle of biofilm resistance. Antimicrob Agents Chemother 45, 999 1007.
38. -δδCT method. Methods 25, 402 408.
39. Lu, L., Hume, M.E. Pillai, S.D. (2004) Autoinducer-2 like activity associated with foods and its interaction with food additives. J Food Prot 67, 1457 1462.
40. Lu, L., Hume, M.E. Pillai, S.D. (2005) Autoinducer-2 like activity on vegetable produce and its potential involvement in bacterial biofilm formation on tomatoes. Foodborne Pathog Dis 2, 242 249.
41. Mahenthiralingam, E., Campbell, M.E. Speert, D.P. (1994) Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun 62, 596 605.
42. Mandalari, G., Bennett, R.N., Bisignano, G., Trombetta, D., Saija, A., Faulds, C.B., Gasson, M.J. Narbad, A. (2007) Antimicrobial activity of flavonoids extracted from bergamot (Citrus bergamia Risso) peel, a byproduct of the essential oil industry. J Appl Microbiol 103, 2056 2064.
43. Miller, E.G., Peacock, J.J., Bourland, T.C., Taylor, S.E., Wright, M.J. Patil, B.S. (2008) Inhibition of oral carcinogenesis by citrus flavonoids. Nutr Cancer 60, 69 74.
44. Mok, K.C., Wingreen, N.S. Bassler, B.L. (2003) Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. EMBO J 22, 870 881.
45. Morin, B., Nichols, L.A., Zalasky, K.M., Davis, J.W., Manthey, J.A. Holland, L.J. (2008) The citrus flavonoids hesperetin and nobiletin differentially regulate low density lipoprotein receptor gene transcription in HepG2 liver cells. J Nutr 138, 1274 1281.
46. Prouty, A.M., Schwesinger, W.H. Gunn, J.S. (2002) Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun 70, 2640 2649.
47. Raman, G., Jayaprakasha, G., Brodbelt, J., Cho, M. Patil, B. (2004) Isolation of structurally similar citrus flavonoids by flash chromatography. Anal Lett 37, 3005 3016.
48. Rasmussen, T.B. Givskov, M. (2006a) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296, 149 161.
49. Rasmussen, T.B. Givskov, M. (2006b) Quorum sensing inhibitors: a bargain of effects. Microbiology 152, 895 904.
50. Rauha, J.-P., Remes, S., Heinonen, M., Hopia, A., Kahkonen, M., Kujala, T., Pihlaja, K., Vuorela, H. et al. (2000) Antimicrobial effects of Finnish plant extracts containing flavonoids and other phenolic compounds. Int J Food Microbiol 56, 3 12.
51. Ren, D., Zuo, R., Gonzalez Barrios, A.F., Bedzyk, L.A., Eldridge, G.R., Pasmore, M.E. Wood, T.K. (2005) Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl Environ Microbiol 71, 4022 4034.
52. Rossi, M., Garavello, W., Talamini, R., Vecchia, C.L., Franceschi, S., Lagiou, P., Zambon, P., Dal, L. et al. (2007) Flavonoids and risk of squamous cell esophageal cancer. Int J Cancer 120, 1560 1564. (Pubitemid 46355394)
53. Rozen, S. Skaletsky, H.J. (2000) Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics Methods and Protocols: Methods in Molecular Biology ed. Krawetz, S. Misener, S. pp. 365 386.
54. Sperandio, V., Torres, A.G., Jarvis, B., Nataro, J.P. Kaper, J.B. (2003) Bacteria-host communication: the language of hormones. Proc Natl Acad Sci USA 100, 8951 8956.
55. Surette, M.G. Bassler, B.L. (1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci USA 95, 7046 7050.
56. Vanamala, J., Reddivari, L., Yoo, K.S., Pike, L.M. Patil, B.S. (2006) Variation in the content of bioactive flavonoids in different brands of orange and grapefruit juices. J Food Compost Anal 19, 157 166.
57. Walters, M. Sperandio, V. (2006) Quorum sensing in Escherichia coli and Salmonella. Int J Med Microbiol 296, 125 131.
58. Waters, C.M. Bassler, B.L. (2006) The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev 20, 2754 2767.
59. Yu, J., Wang, L., Walzem, R.L., Miller, E.G., Pike, L.M. Patil, B.S. (2005) Antioxidant activity of citrus limonoids, flavonoids, and coumarins. J Agric Food Chem 53, 2009 2014.