Molecular mechanisms of compounds affecting bacterial biofilm formation and dispersal

Applied Microbiology and Biotechnology

Volumn 86, Issue 3, 2010, Pages 813-823

  Landini, Paolo ^a   Antoniani, Davide ^a   Burgess, J Grant ^b   Nijland, Reindert ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Antimicrobial drugs; Biofilm formation and dispersal; C di GMP; Quorumsensing; Structure directed screening; Target directed screening

Indexed keywords

ANTI-BIOFILM; ANTIBIOTIC TREATMENT; ANTIMICROBIAL DRUG; BACTERIAL BIOFILM; BACTERIAL COMMUNITY; BIOFILM DEVELOPMENT; BIOFILM FORMATION; BIOFILM INHIBITORS; CELLULAR PROCESS; CHRONIC INFECTION; EXTRA-CELLULAR POLYMERIC SUBSTANCES; MATRIX; MODE OF ACTION; MOLECULAR MECHANISM; PATHOGENIC BACTERIUM; QUORUM-SENSING; SCREENING TARGETS; SELECTED EXAMPLES; SIGNAL MOLECULES; SINGLE CELLS; SOLID SURFACE; VIRULENCE FACTORS;

BACTERIA; BACTERIOLOGY; BIOCHEMISTRY; BIOFILTERS; METABOLISM; TARGETS;

BIOFILMS;

ANTIINFECTIVE AGENT; BROMOAGELIFERIN; DISPERSIN B; DNA; FURANONE DERIVATIVE; GUANOSINE PHOSPHATE; OROIDIN; TRICLOSAN; UNCLASSIFIED DRUG;

ANTIBIOTICS; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; DRUG; METABOLISM; MICROBIAL ACTIVITY; PATHOGEN; VIRULENCE;

ANTIBACTERIAL ACTIVITY; BIOFILM; DNA REPLICATION; DNA SYNTHESIS INHIBITION; DRUG INHIBITION; DRUG MECHANISM; DRUG SCREENING; DRUG STRUCTURE; GRAM NEGATIVE INFECTION; GRAM POSITIVE BACTERIUM; NONHUMAN; NUCLEOTIDE METABOLISM; SHORT SURVEY; SKIN INFECTION; WOUND INFECTION;

ANTI-BACTERIAL AGENTS; BACTERIA; BIOFILMS; CYCLIC GMP; DNA; NUCLEOTIDES; QUORUM SENSING;

BACTERIA (MICROORGANISMS);

EID: 77950629120     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-010-2468-8     Document Type: Short Survey

References (118)

1. Abdelnour A, Arvidson S, Bremell T, Rydén C, Tarkowski A (1993) The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect Immun 61:3879-3885 (Pubitemid 23260062)
2. Abraham WR (2006) Controlling biofilms of gram-positive pathogenic bacteria. Curr Med Chem 13:1509-1524
3. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, Kjelleberg S, Molin S, Givskov M, Tolker-Nielsen T (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59:1114-1128
4. Amara N, Mashiach R, Amar D, Krief P, Spieser SA, Bottomley MJ, Aharoni A, Meijler MM (2009) Covalent inhibition of bacterial quorum sensing. J Am Chem Soc 131:10610-10619
5. Anderl JN, Franklin MJ, Stewart PS (2000) Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44:1818-1824
6. Anderson GG, O'Toole GA (2008) Innate and induced resistance mechanisms of bacterial biofilms. Curr Top Microbiol Immunol 322:85-105
7. Ando T, Suzuki H, Nishimura S, Tanaka T, Hiraishi A, Kikuchi Y (2006) Characterization of extracellular RNAs produced by the marine photosynthetic bacterium Rhodovulum sulfidophilum. J Biochem 139:805-811 (Pubitemid 43973928)
8. Antoniani D, Bocci P, Maciag A, Raffaelli N, Landini P (2010) Monitoring of di-guanylate cyclase activity and of cyclic-di-GMP biosynthesis by whole-cell assays suitable for high-throughput screening of biofilm inhibitors. Appl Microbiol Biotechnol 85:1095-1104
9. Attila C, Ueda A, Wood TK (2009) 5-Fluorouracil reduces biofilm formation in Escherichia coli K-12 through global regulator AriR as an antivirulence compound. Appl Microbiol Biotechnol 82:525-533
10. Balaban N, Novick RP (1995) Autocrine regulation of toxin synthesis by Staphylococcus aureus. Proc Natl Acad Sci USA 92:1619-1623
11. Balaban N, Gov Y, Giacometti A, Cirioni O, Ghiselli R, Mocchegiani F, Orlando F, D'Amato G, Saba V, Scalise G, Bernes S, Mor A (2004) A chimeric peptide composed of a dermaseptin derivative and an RNA III-inhibiting peptide prevents graft-associated infections by antibiotic-resistant staphylococci. Antimicrob Agents Chemother 48:2544-2550 (Pubitemid 38823423)
12. Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJ, Slater H, Dow JM, Williams P, Daniels MJ (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555-566 (Pubitemid 27241703)
13. Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344-7353 (Pubitemid 44646233)
14. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic diguanosine-5′- monophosphate levels and enhanced dispersal. J Bacteriol 191:7333-7342
15. Bjarnsholt T, Jensen PØ, Rasmussen TB, Christophersen L, Calum H, Hentzer M, Hougen H, Rygaard J, Moser C, Eberl L, Høiby N, Givskov M (2005) Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infection. Microbiology 151:3873-3880 (Pubitemid 41829968)
16. Boehm A, Steiner S, Zaehringer F, Casanova A, Hamburger F, Ritz D, Keck W, Ackermann M, Schirmer T, Jenal U (2009) Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol 72:1500-1516
17. Boles BR, Horswill AR (2008) Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052 Boyd A, Chakrabarty AM (1994) Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl Environ Microbiol 60:2355-2359
18. Burke C, Thomas T, Egan S, Kjelleberg S (2007) The use of functional genomics for the identification of a gene cluster encoding for the biosynthesis of an antifungal tambjamine in the marine bacterium Pseudoalteromonas tunicata. Environ Microbiol 9:814-818 (Pubitemid 46246588)
19. Carté B, Faulkner DJ (1986) Role of secondary metabolites in feeding associations between a predatory nudibranch, two grazing nudibranchs and a bryozoan. J Chem Ecol 12:795-804
20. Cashel M, Gentry DR, Hernandez VJ, Vinella D (1996) The stringent response. In: Neidhardt FC, Curtiss R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff W, Riley M, Schaechter M, Umbarger AE (eds) Escherichia coli and Salmonella typhimurium cellular and molecular biology. American Society ofMicrobiology, Washington, pp 1458-1496
21. Ceri H, Olson M, Morck D, Storey D, Read R, Buret A, Olson B (2001) The MBEC Assay System: multiple equivalent biofilms for antibiotic and biocide susceptibility testing. Methods Enzymol 337:377-385 (Pubitemid 32691309)
22. Chan C, Paul R, Samoray D, Amiot NC, Giese B, Jenal U, Schirmer T (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101:17084-17089 (Pubitemid 39627778)
23. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin- Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711-745
24. Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67:5427-5433 (Pubitemid 29455321)
25. Darouiche RO, Mansouri MD, Gawande PV, Madhyastha S (2009) Antimicrobial and antibiofilm efficacy of triclosan and dispersinB combination. J Antimicrob Chemother 64:88-93
26. Davies DG, Marques CN (2009) A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393-1403
27. De N, Pirruccello M, Krasteva PV, Bae N, Raghavan RV, Sondermann H (2008) Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol 6:e67 (Pubitemid 351485604)
28. Donelli G, Francolini I, Romoli D, Guaglianone E, Piozzi A, Ragunath C, Kaplan JB (2007) Synergistic activity of dispersinB and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes. Antimicrob Agents Chemother 51:2733-2740 (Pubitemid 47206207)
29. Dong YH, Gusti AR, Zhang Q, Xu JL, Zhang LH (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754-1759 (Pubitemid 34279982)
30. Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci USA 100:10995-11000 (Pubitemid 37140141)
31. Fuqua C, Winans SC, Greenberg EP (1996) Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol 50:727-751 (Pubitemid 26337480)
32. Galperin MY (2004) Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6:552-567
33. Geske GD, O'Neill JC, Miller DM, Mattmann ME, Blackwell HE (2007) Modulation of bacterial quorum sensing with synthetic ligands: systematic evaluation of N-acylated homoserine lactones in multiple species and new insights into their mechanisms of action. J Am Chem Soc 129:13613-13625
34. Giacometti A, Cirioni O, Gov Y, Ghiselli R, Del Prete MS, Mocchegiani F, Saba V, Orlando F, Scalise G, Balaban N, Dell'Acqua G (2003) RNA III inhibiting peptide inhibits in vivo biofilm formation by drug-resistant Staphylococcus aureus. Antimicrob Agents Chemother 47:1979-1983 (Pubitemid 36637826)
35. Gjermansen M, Ragas P, Sternberg C, Molin S, Tolker-Nielsen T (2005) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ Microbiol 7:894-906 (Pubitemid 40697647)
36. Gotoh H, Zhang Y, Dallo SF, Hong S, Kasaraneni N, Weitao T (2008) Pseudomonas aeruginosa, under DNA replication inhibition, tends to form biofilms via Arr. Res Microbiol 159:294-302
37. Guiton PS, Hung CS, Kline KA, Roth R, Kau AL, Hayes E, Heuser J, Dodson KW, Caparon MG, Hultgren SJ (2009) Contribution of autolysin and Sortase a during Enterococcus faecalis DNAdependent biofilm development. Infect Immun 77:3626-3638
38. Hammer BK, Bassler BL (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50:101-104
39. Hegde M, Wood TK, Jayaraman A (2009) The neuroendocrine hormone norepinephrine increases Pseudomonas aeruginosa PA14 virulence through the las quorum-sensing pathway. Appl Microbiol Biotechnol 84:763-776
40. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, Kjelleberg S, Givskov M (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87-102 (Pubitemid 34083188)
41. Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112:1300-1307 (Pubitemid 38057681)
42. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Costerton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Høiby N, Givskov M (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803-3815 (Pubitemid 36975709)
43. Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI (2005) Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436:1171-1175 (Pubitemid 41232296)
44. Hoffmann N, Lee B, Hentzer M, Rasmussen TB, Song Z, Johansen HK, Givskov M, Høiby N (2007) Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr(-/-) mice. Antimicrob Agents Chemother 51:3677-3687
45. Holland LM, O'Donnell ST, Ryjenkov DA, Gomelsky L, Slater SR, Fey PD, Gomelsky M, O'Gara JP (2008) A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J Bacteriol 190:5178-5189
46. Horswill AR, Stoodley P, Stewart PS, Parsek MR (2007) The effect of the chemical, biological, and physical environment on quorum sensing in structured microbial communities. Anal Bioanal Chem 387:371-380
47. Huigens RW 3rd, Ma L, Gambino C, Moeller PD, Basso A, Cavanagh J, Wozniak DJ, Melander C (2008) Control of bacterial biofilms with marine alkaloid derivatives. Mol Biosyst 4:614-621 (Pubitemid 351706305)
48. Iauk L, Lo Bue AM, Milazzo I, Rapisarda A, Blandino G (2003) Antibacterial activity of medicinal plant extracts against periodontopathic bacteria. Phytother Res 17:599-604 (Pubitemid 36781732)
49. Ichimiya T, Takeoka K, Hiramatsu K, Hirai K, Yamasaki T, Nasu M (1996) The influence of azithromycin on the biofilm formation of Pseudomonas aeruginosa in vitro. Chemotherapy 42:186-191 (Pubitemid 26095173)
50. Izano EA, Sadovskaya I, Vinogradov E, Mulks MH, Velliyagounder K, Ragunath C, Kher WB, Ramasubbu N, Jabbouri S, Perry MB, Kaplan JB (2007) Poly-N-acetylglucosamine mediates biofilm formation and antibiotic resistance in Actinobacillus pleuropneumoniae. Microb Pathog 43:1-9 (Pubitemid 46678642)
51. James SG, Holmström C, Kjelleberg S (1996) Purification and characterization of a novel antibacterial protein from the marine bacterium D2. Appl Environ Microbiol 62:2783-2788 (Pubitemid 26260079)
52. Janzon L, Arvidson S (1990) The role of the δ-gene (hld) in the regulation of virulence genes by the accessory gene regulator (agr) in Staphylococcus aureus. EMBO J 9:1391-1399 (Pubitemid 20136992)
53. Junker LM, Clardy J (2007) High-throughput screens for smallmolecule inhibitors of Pseudomonas aeruginosa biofilm development. Antimicrob Agents Chemother 51:3582-3590 (Pubitemid 47519347)
54. Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177:3998-4008
55. Kaplan JB, Ragunath C, Ramasubbu N, Fine DH (2003) Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous β-hexosaminidase activity. J Bacteriol 185:4693-4698 (Pubitemid 36962275)
56. Karatan E, Watnick PI (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310-347
57. Kiran MD, Adikesavan NV, Cirioni O, Giacometti A, Silvestri C, Scalise G, Ghiselli R, Saba V, Orlando F, Shoham M, Balaban N (2008) Discovery of a quorum-sensing inhibitor of drug-resistantstaphylococcal infections by structure-based virtual screening. Mol Pharmacol 73:1578-1586 (Pubitemid 351574847)
58. Kong KF, Vuong C, Otto M (2006) Staphylococcus quorum sensing in biofilm formation and infection. Int J Med Microbiol 296:133-139 (Pubitemid 43375996)
59. König GM, Kehraus S, Seibert SF, Abdel-Lateff A, Müller D (2006) Natural products from marine organisms and their associated microbes. ChemBioChem 7:229-238 (Pubitemid 43220933)
60. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Asubel FM, Lory S (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103:2839-2844
61. Lewis K (2008) Multidrug tolerance of biofilms and persister cells. Curr Top Microbiol Immunol 322:107-131
62. Li M, Ni N, Chou HT, Lu CD, Tai PC, Wang B (2008) Structurebased discovery and experimental verification of novel AI-2 quorum sensing inhibitors against Vibrio harveyi. ChemMed-Chem 3:1242-1249
63. Li YH, Tang N, Aspiras MB, Lau PC, Lee JH, Ellen RP, Cvitkovitch DG (2002) A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J Bacteriol 184:2699-2708 (Pubitemid 34457037)
64. Lönn-Stensrud J, Landin MA, Benneche T, Petersen FC, Scheie AA (2009) Furanones, potential agents for preventing Staphylococcus epidermidis biofilm infections? J Antimicrob Chemother 63:309-316
65. Mai-Prochnow A, Lucas-Elio P, Egan S, Thomas T, Webb JS, Sanchez-Amat A, Kjelleberg S (2008) Hydrogen peroxide linked to lysine oxidase activity facilitates biofilm differentiation and dispersal in several gram-negative bacteria. J Bacteriol 190:5493-5501
66. Manefield M, Rasmussen TB, Henzter M, Andersen JB, Steinberg P, Kjelleberg S, Givskov M (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 118:1119-1127
67. Marketon MM, Glenn SA, Eberhard A, González JE (2003) Quorum sensing controls exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 185:325-331
68. McKnight SL, Iglewski BH, Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 182:2702-2708
69. McLennan MK, Ringoir DD, Frirdich E, Svensson SL, Wells DH, Jarrell H, Szymanski CM, Gaynor EC (2008) Campylobacter jejuni biofilms up-regulated in the absence of the stringent response utilize a calcofluor white-reactive polysaccharide. J Bacteriol 190:1097-1107
70. Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol l55:165-199
71. Mizukane R, Hirakata Y, Kaku M, Ishii Y, Furuya N, Ishida K, Koga H, Kohno S, Yamaguchi K (1994) Comparative in vitro exoenzyme-suppressing activities of azithromycin and other macrolide antibiotics against Pseudomonas aeruginosa. Antimicrob Agents Chemother 38:528-533
72. Morgan R, Kohn D, Hwang SH, Hassett DJ, Sauer K (2006) BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol 188:7335-7343
73. Müh U, Schuster M, Heim R, Singh A, Olson ER, Greenberg EP (2006) Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Chemother 50:3674-3679
74. Muto Y, Goto S (1986) Transformation by extracellular DNA produced by Pseudomonas aeruginosa. Microbiol Immunol 30:621-628
75. Nalca Y, Jänsch L, Bredenbruch F, Geffers R, Buer J, Häussler S (2006) Quorum-sensing antagonistic activities of azithromycin in Pseudomonas aeruginosa PAO1: a global approach. Antimicrob Agents Chemother 50:1680-1688
76. Njoroge J, Sperandio J (2009) Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Molec Med 1:201-210
77. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12:3967-3975
78. Nucleo E, Steffanoni L, Fugazza G, Migliavacca R, Giacobone E, Navarra A, Pagani L, Landini P (2009) Growth in glucose-based medium and exposure to subinhibitory concentrations of imipenem induce biofilm formation in a multidrug-resistant clinical isolate of Acinetobacter baumannii. BMC Microbiol 9:270
79. Odenholt I (2001) Pharmacodynamic effects of subinhibitory antibiotic concentrations. Int J Antimicrob Agents 17:1-8
80. Ozer EA, Pezzulo A, Shih DM, Chun C, Furlong C, Lusis AJ, Greenberg EP, Zabner J (2005) Human and murine paraoxonase 1 are host modulators of Pseudomonas aeruginosa quorumsensing. FEMS Microbiol Lett 253:29-37
81. Park SY, Kang HO, Jang HS, Lee JK, Koo BT, Yum DY (2005) Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microbiol 71:2632-2641
82. Paul VJ, Lindquist N, Fenical W (1990) Chemical defences of the tropical ascidian Atapozoa-sp. and its nudibranch predators Nembrotha-spp. Mar Ecol Prog Ser 59:109-118
83. Persson T, Hansen TH, Rasmussen TB, Skindersø ME, Givskov M, Nielsen J (2005) Rational design and synthesis of new quorumsensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 3:253-262
84. Pratten J, Foster SJ, Chan PF, Wilson M, Nair SP (2001) Staphylococcus aureus accessory regulators: expression within biofilms and effect on adhesion. Microbes Infect 3:633-637 (Pubitemid 32607758)
85. Qin Z, Yang L, Qu D, Molin S, Tolker-Nielsen T (2009) Pseudomonas aeruginosa extracellular products inhibit staphylococcal growth, and disrupt established biofilms produced by Staphylococcus epidermidis. Microbiology 155:2148-2156
86. Rasmussen TB, Skindersoe ME, Bjarnsholt T, Phipps RK, Christensen KB, Jensen PO, Andersen JB, Koch B, Larsen TO, Hentzer M, Eberl L, Hoiby N, Givskov M (2005) Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325-1340 (Pubitemid 40711780)
87. Recsei P, Kreiswirth B, O'Reilly M, Schlievert P, Gruss A, Novick RP (1986) Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol Gen Genet 202:58-61 (Pubitemid 16150393)
88. Ren D, Bedzyk LA, Setlow P, England DF, Kjelleberg S, Thomas SM, Ye RW, Wood TK (2004) Differential gene expression to investigate the effect of (5Z)-4-bromo-5-(bromomethylene)-3- butyl-2(5H)-furanone on Bacillus subtilis. Appl Environ Microbiol 70:4941-4949 (Pubitemid 39095524)
89. Richards JJ, Ballard TE, Huigens RW 3rd, Melander C (2008) Synthesis and screening of an oroidin library against Pseudomonas aeruginosa biofilms. Chembiochem 9:1267-1279
90. Rivardo F, Turner RJ, Allegrone G, Ceri H, Martinotti MG (2009) Anti-adhesion activity of two biosurfactants produced by Bacillus spp. prevents biofilm formation of human bacterial pathogens. Appl Microbiol Biotechnol 83:541-553
91. Rogers SA, Krayer M, Lindsey JS, Melander C (2009) Tandem dispersion and killing of bacteria from a biofilm. Org Biomol Chem 7:603-606
92. Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P(2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312-7326 (Pubitemid 39383116)
93. Simm R, Morr M, Kader A, Nimtiz M, Römling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123-1134 (Pubitemid 39120434)
94. Smith KM, Bu Y, Suga H (2003) Induction and inhibition of Pseudomonas aeruginosa quorum sensing by synthetic autoinducer analogs. Chem Biol 10:81-89 (Pubitemid 36154477)
95. Smith RS, Iglewski BH (2003) Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. J Clin Invest 112:1460-1465 (Pubitemid 38056270)
96. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321:411-413 (Pubitemid 352029978)
97. Svitil AL, Cashel M, Zyskind JW (1993) Guanosine tetraphosphate inhibits protein synthesis in vivo. A possible protective mechanism for starvation stress in Escherichia coli. J Biol Chem 268:2307-2311 (Pubitemid 23057843)
98. Tamayo R, Pratt JT, Camilli A (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61:131-148 (Pubitemid 350058203)
99. Tateda K, Comte R, Pechere JC, Köhler T, Yamaguchi K, Van Delden C (2001) Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 45:1930-1933 (Pubitemid 32466379)
100. Thormann KM, Saville RM, Shukla S, Spormann AM (2005) Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol 187:1014-1021 (Pubitemid 40189775)
101. Thormann K, Duttler MS, Saville RM, Hyodo M, Shukla S, Hayakawa Y, Spormann AM (2006) Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J Bacteriol 188:2681-2691
102. Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483
103. Ueda A, Attila C, Whiteley M, Wood TK (2009) Uracil influences quorum sensing and biofilm formation in Pseudomonas aeruginosa and fluorouracilnis an antagonist. Microb Biotechnol 2:62-74
104. Uroz S, Heinonsalo J (2008) Degradation of N-acyl homoserine lactone quorum sensing signal molecules by forest rootassociated fungi. FEMS Microbiol Ecol 65:271-278 (Pubitemid 351989225)
105. Vilain S, Pretorius JM, Theron J, Brozel VS (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75:2861-2868
106. Vuong C, Gerke C, Somerville GA, Fischer ER, Otto M (2003) Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J Infect Dis 188:706-718 (Pubitemid 37115184)
107. Wagner VE, Gillis RJ, Iglewski BH (2004) Transcriptome analysis of quorum-sensing regulation and virulence factor expression in Pseudomonas aeruginosa. Vaccine 6(22 Suppl 1):S15-20
108. Wagner VE, Li LL, Isabella VM, Iglewski BH (2007) Analysis of the hierarchy of quorum-sensing regulation in Pseudomonas aeruginosa. Anal Bioanal Chem 387:469-479 (Pubitemid 46067462)
109. Wang LH, He Y, Gao Y, Wu JE, Dong YH, He C, Wang SX, Weng LX, Xu JL, Tay L, Fang RX, Zhang LH (2004a) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51:903-912 (Pubitemid 38233953)
110. Wang X, Preston JF 3rd, Romeo T (2004b) The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186:2724-2734 (Pubitemid 38525927)
111. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R (2006) Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 62:1014-1034 (Pubitemid 44655315)
112. Weinhouse H, Sapir S, Amikam D, Shilo Y, Volman G, Ohana P, Benziman M (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416:207-211 (Pubitemid 27462790)
113. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295:1487 (Pubitemid 34173996)
114. Xu L, Li H, Vuong C, Vadyvaloo V, Wang J, Yao Y, Otto M, Gao Q (2006) Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect Immun 74:488-496 (Pubitemid 43023104)
115. Yang L, Rybtke MT, Jakobsen TH, Hentzer M, Bjarnsholt T, Givskov M, Tolker-Nielsen T (2009) Computer-aided identification of recognized drugs as Pseudomonas aeruginosa quorum-sensing inhibitors. Antimicrob Agents Chemother 53:2432-2443
116. Yarwood JM, Bartels DJ, Volper EM, Greenberg EP (2004) Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186:1838-1850 (Pubitemid 38314529)
117. Zeng Z, Qian L, Cao L, Tan H, Huang Y, Xue X, Shen Y, Zhou S (2008) Virtual screening for novel quorum sensing inhibitors to eradicate biofilm formation of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 79:119-126
118. Zhu H, Kumar A, Ozkan J, Bandara R, Ding A, Perera I, Steinberg P, Kumar N, Lao W, Griesser SS, Britcher L, Griesser HJ, Willcox MD (2008) Fimbrolide-coated antimicrobial lenses: their in vitro and in vivo effects. Optom Vis Sci 85:292-300 (Pubitemid 351643366)