The hierarchy quorum sensing network in Pseudomonas aeruginosa

Abe A, Matsuzawa T, Kuwae A (2005) Type-III effectors: sophisticated bacterial virulence factors. C R Biol 328:413–428

Adam EC, Mitchell BS, Schumacher DU, Grant G, Schumacher U (1997) Pseudomonas aeruginosa II lectin stops human ciliary beating: therapeutic implications of fucose. Am J Respir Crit Care Med 155:2102–2104

Albus AM, Pesci EC, Runyen-Janecky LJ, West SE, Iglewski BH (1997) Vfr controls quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3928–3935

Anba J, Bidaud M, Vasil ML, Lazdunski A (1990) Nucleotide sequence of the Pseudomonas aeruginosa phoB gene, the regulatory gene for the phosphate regulon. J Bacteriol 172:4685–4689

Bains M, Fernandez L, Hancock RE (2012) Phosphate starvation promotes swarming motility and cytotoxicity of Pseudomonas aeruginosa. Appl Environ Microbiol 78:6762–6768

Baysse C, Cullinane M, Dénervaud V, Burrowes E, Dow JM, Morrissey JP, Tam L, Trevors JT, O’Gara F (2005) Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 151:2529–2542

Bertani I, Venturi V (2004) Regulation of the N-acyl homoserine lactone-dependent quorum-sensing system in rhizosphere Pseudomonas putida WCS358 and cross-talk with the stationary-phase RpoS sigma factor and the global regulator GacA. Appl Environ Microbiol 70:5493–5502

Blier A-S, Veron W, Bazire A, Gerault E, Taupin L, Vieillard J, Rehel K, Dufour A, Le Derf F, Orange N (2011) C-type natriuretic peptide modulates quorum sensing molecule and toxin production in Pseudomonas aeruginosa. Microbiology 157:1929–1944

Bonomo RA, Szabo D (2006) Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clinical Infectious Diseases 43(Suppl 2):S49–S56

Borlee BR, Geske GD, Blackwell HE, Handelsman J (2010) Identification of synthetic inducers and inhibitors of the quorum-sensing regulator LasR in Pseudomonas aeruginosa by high-throughput screening. Appl Environ Microbiol 76:8255–8258

Branny P, Pearson JP, Pesci EC, Kohler T, Iglewski BH, Van Delden C (2001) Inhibition of quorum sensing by a Pseudomonas aeruginosa dksA homologue. J Bacteriol 183:1531–1539

Brint JM, Ohman DE (1995) Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. Journal of Bacteriology 177:7155–7163

Cabrol S, Olliver A, Pier GB, Andremont A, Ruimy R (2003) Transcription of quorum-sensing system genes in clinical and environmental isolates of Pseudomonas aeruginosa. J Bacteriol 185:7222–7230

Camilli A, Bassler BL (2006) Bacterial small-molecule signaling pathways. Science 311:1113–1116

Campodonico VL, Gadjeva M, Paradis-Bleau C, Uluer A, Pier GB (2008) Airway epithelial control of Pseudomonas aeruginosa infection in cystic fibrosis. Trends Mol Med 14:120–133

Cao JG, Meighen EA (1993) Biosynthesis and stereochemistry of the autoinducer controlling luminescence in Vibrio harveyi. J Bacteriol 175:3856–3862

Cao H, Krishnan G, Goumnerov B, Tsongalis J, Tompkins R, Rahme LG (2001) A quorum sensing-associated virulence gene of Pseudomonas aeruginosa encodes a LysR-like transcription regulator with a unique self-regulatory mechanism. Proc Natl Acad Sci USA 98:14613–14618

Castric PA (1983) Hydrogen cyanide production by Pseudomonas aeruginosa at reduced oxygen levels. Can J Microbiol 29:1344–1349

Castric P (1994) Influence of oxygen on the Pseudomonas aeruginosa hydrogen cyanide synthase. Curr Microbiol 29:19–21

Castric PA, Ebert RF, Castric KF (1979) The relationship between growth phase and cyanogenesis in Pseudomonas aeruginosa. Curr Microbiol 2:287–292

Chernish RN, Aaron SD (2003) Approach to resistant gram-negative bacterial pulmonary infections in patients with cystic fibrosis. Curr Opin Pulm Med 9:509–515

Chugani S, Greenberg E (2007) The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microbial pathogenesis 42:29–35

Chugani SA, Whiteley M, Lee KM, D’Argenio D, Manoil C, Greenberg EP (2001) QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 98:2752–2757

Ciofu O, Mandsberg LF, Bjarnsholt T, Wassermann T, Høiby N (2010) Genetic adaptation of Pseudomonas aeruginosa during chronic lung infection of patients with cystic fibrosis: strong and weak mutators with heterogeneous genetic backgrounds emerge in mucA and/or lasR mutants. Microbiology 156:1108–1119

Coleman JP, Hudson LL, McKnight SL, Farrow JM, Calfee MW, Lindsey CA, Pesci EC (2008) Pseudomonas aeruginosa PqsA is an anthranilate-coenzyme A ligase. J Bacteriol 190:1247–1255

Collier DN, Anderson L, McKnight SL, Noah TL, Knowles M, Boucher R, Schwab U, Gilligan P, Pesci EC (2002) A bacterial cell to cell signal in the lungs of cystic fibrosis patients. FEMS Microbiol Lett 215:41–46

Cook JMI, Harragan B (1992) In: Proceedings of the 92nd annual meeting of the american society for microbiology. Paper presented at 92nd annual meeting of the american society for microbiology, New Orleans

Cornforth JW, James AT (1956) Structure of a naturally occurring antagonist of dihydrostreptomycin. The Biochemical Journal 63:124–130

Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci 3(4):220–227

Costerton JW (2001) Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol 9:50–52

Daddaoua A, Fillet S, Fernández M, Udaondo Z, Krell T, Ramos JL (2012) Genes for carbon metabolism and the ToxA virulence factor in Pseudomonas aeruginosa are regulated through molecular interactions of PtxR and PtxS. PLoS One 7:e39390

D’Argenio DA, Calfee MW, Rainey PB, Pesci EC (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184:6481–6489

D’Argenio DA, Wu M, Hoffman LR, Kulasekara HD, Deziel E, Smith EE, Nguyen H, Ernst RK, Larson Freeman TJ, Spencer DH et al (2007) Growth phenotypes of Pseudomonas aeruginosa lasR mutants adapted to the airways of cystic fibrosis patients. Mol Microbiol 64:512–533

de Kievit T, Seed PC, Nezezon J, Passador L, Iglewski BH (1999) RsaL, a novel repressor of virulence gene expression in Pseudomonas aeruginosa. J Bacteriol 181:2175–2184

Dekimpe V, Deziel E (2009) Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712–723

Denervaud V, TuQuoc P, Blanc D, Favre-Bonte S, Krishnapillai V, Reimmann C, Haas D, van Delden C (2004) Characterization of cell-to-cell signaling-deficient Pseudomonas aeruginosa strains colonizing intubated patients. J Clin Microbiol 42:554–562

Deng Y, Wu J, Tao F, Zhang LH (2011) Listening to a new language: DSF-based quorum sensing in Gram-negative bacteria. Chem Rev 111:160–173

Denning GM, Wollenweber LA, Railsback MA, Cox CD, Stoll LL, Britigan BE (1998) Pseudomonas pyocyanin increases interleukin-8 expression by human airway epithelial cells. Infect Immun 66:5777–5784

Deziel E, Lepine F, Milot S, He J, Mindrinos MN, Tompkins RG, Rahme LG (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA 101:1339–1344

Déziel E, Gopalan S, Tampakaki AP, Lépine F, Padfield KE, Saucier M, Xiao G, Rahme LG (2005) The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-l-homoserine lactones. Mol Microbiol 55:998–1014

Diggle SP, Winzer K, Lazdunski A, Williams P, Camara M (2002) Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J Bacteriol 184:2576–2586

Diggle SP, Winzer K, Chhabra SR, Worrall KE, Cámara M, Williams P (2003) The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol Microbiol 50:29–43

Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR, Lamont IL, Kong X, Hider RC, Cornelis P, Cámara M (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14:87–96

Doshi HK, Chua K, Kagda F, Tambyah PA (2011) Multi drug resistant pseudomonas infection in open fractures post definitive fixation leading to limb loss: a report of three cases. International Journal of Case Reports and Images (IJCRI) 2:1–6

Dubern JF, Diggle SP (2008) Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol Biosyst 4:882–888

Eberhard A (1972) Inhibition and activation of bacterial luciferase synthesis. J Bacteriol 109:1101–1105

Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ (1981) Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449

Farrow JM 3rd, Sund ZM, Ellison ML, Wade DS, Coleman JP, Pesci EC (2008) PqsE functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 190:7043–7051

Filloux A, Bally M, Soscia C, Murgier M, Lazdunski A (1988) Phosphate regulation in Pseudomonas aeruginosa: cloning of the alkaline phosphatase gene and identification of phoB-and phoR-like genes. Mol Gen Genet 212:510–513

Frisk A, Schurr JR, Wang G, Bertucci DC, Marrero L, Hwang SH, Hassett DJ, Schurr MJ (2004) Transcriptome analysis of Pseudomonas aeruginosa after interaction with human airway epithelial cells. Infect Immun 72:5433–5438

Fuqua C (2006) The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J Bacteriol 188:3169–3171

Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275

Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472–6480

Gambello MJ, Iglewski BH (1991) Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 173:3000–3009

Gambello MJ, Kaye S, Iglewski BH (1993) LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect Immun 61:1180–1184

Gentry DR, Cashel M (1996) Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol Microbiol 19:1373–1384

Haddad A, Jensen V, Becker T, Haussler S (2009) The Pho regulon influences biofilm formation and type three secretion in Pseudomonas aeruginosa. Environ Microbiol Rep 1:488–494

Hamood AN, Griswold J, Colmer J (1996) Characterization of elastase-deficient clinical isolates of Pseudomonas aeruginosa. Infect Immun 64:3154–3160

Hauser AR, Cobb E, Bodí M, Mariscal D, Vallés J, Engel JN, Rello J (2002) Type III protein secretion is associated with poor clinical outcomes in patients with ventilator-associated pneumonia caused by Pseudomonas aeruginosa. Crit Care Med 30:521–528

Henry RL, Mellis CM, Petrovic L (1992) Mucoid Pseudomonas aeruginosa is a marker of poor survival in cystic fibrosis. Pediatr Pulmonol 12:158–161

Hense BA, Kuttler C, Muller J, Rothballer M, Hartmann A, Kreft JU (2007) Does efficiency sensing unify diffusion and quorum sensing? Nature Rev Microbiol 5:230–239

Heurlier K, Dénervaud V, Pessi G, Reimmann C, Haas D (2003) Negative control of quorum sensing by RpoN (σ54) in Pseudomonas aeruginosa PAO1. J Bacteriol 185:2227–2235

Hoffman LR, Kulasekara HD, Emerson J, Houston LS, Burns JL, Ramsey BW, Miller SI (2009) Pseudomonas aeruginosa lasR mutants are associated with cystic fibrosis lung disease progression. J Cyst Fibros 8:66–70

Hsieh Y-J, Wanner BL (2010) Global regulation by the seven-component Pi signaling system. Curr Opin Microbiol 13:198–203

Huang JJ, Petersen A, Whiteley M, Leadbetter JR (2006) Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 72:1190–1197

Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62:379–433

Jackowski JT, Szepfalusi Z, Wanner DA, Seybold Z, Sielczak MW, Lauredo IT, Adams T, Abraham WM, Wanner A (1991) Effects of P. aeruginosa-derived bacterial products on tracheal ciliary function: role of O2 radicals. Am J Physiol 260:L61–L67

Jackson AA, Gross MJ, Daniels EF, Hampton TH, Hammond JH, Vallet-Gely I, Dove SL, Stanton BA, Hogan DA (2013) Anr and its activation by PlcH activity in Pseudomonas aeruginosa host colonization and virulence. J Bacteriol 195:3093–3104

Jensen V, Löns D, Zaoui C, Bredenbruch F, Meissner A, Dieterich G, Münch R, Häussler S (2006) RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and-independent pathways. J Bacteriol 188:8601–8606

Jones S, Yu B, Bainton NJ, Birdsall M, Bycroft BW, Chhabra SR, Cox AJ, Golby P, Reeves PJ, Stephens S et al (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12:2477–2482

Joseleau-Petit D, Vinella D, D’Ari R (1999) Metabolic alarms and cell division in Escherichia coli. J Bacteriol 181:9–14

Jude F, Kohler T, Branny P, Perron K, Mayer MP, Comte R, van Delden C (2003) Posttranscriptional control of quorum-sensing-dependent virulence genes by DksA in Pseudomonas aeruginosa. J Bacteriol 185:3558–3566

Juhas M, Wiehlmann L, Huber B, Jordan D, Lauber J, Salunkhe P, Limpert AS, von Gotz F, Steinmetz I, Eberl L et al (2004) Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831–841

Kessler E, Safrin M, Olson JC, Ohman DE (1993) Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268:7503–7508

Kim EJ, Sabra W, Zeng AP (2003) Iron deficiency leads to inhibition of oxygen transfer and enhanced formation of virulence factors in cultures of Pseudomonas aeruginosa PAO1. Microbiology 149:2627–2634

Kiratisin P, Tucker KD, Passador L (2002) LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J Bacteriol 184:4912–4919

Konings AF, Martin LW, Sharples KJ, Roddam LF, Latham R, Reid DW, Lamont IL (2013) Pseudomonas aeruginosa uses multiple pathways to acquire iron during chronic infection in cystic fibrosis lungs. Infect Immun 81:2697–2704

Kosorok MR, Zeng L, West SE, Rock MJ, Splaingard ML, Laxova A, Green CG, Collins J, Farrell PM (2001) Acceleration of lung disease in children with cystic fibrosis after Pseudomonas aeruginosa acquisition. Pediatr Pulmonol 32:277–287

Krieg DP, Helmke RJ, German VF, Mangos JA (1988) Resistance of mucoid Pseudomonas aeruginosa to nonopsonic phagocytosis by alveolar macrophages in vitro. Infect Immun 56:3173–3179

Laarman AJ, Bardoel BW, Ruyken M, Fernie J, Milder FJ, van Strijp JA, Rooijakkers SH (2012) Pseudomonas aeruginosa alkaline protease blocks complement activation via the classical and lectin pathways. J Immunol 188:386–393

Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GS, Lazdunski A, Williams P (1995) Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol 17:333–343

Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A (1996) A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 21:1137–1146

Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D (2004) Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect Immun 72:4275–4278

Ledgham F, Soscia C, Chakrabarty A, Lazdunski A, Foglino M (2003a) Global regulation in Pseudomonas aeruginosa: the regulatory protein AlgR2 (AlgQ) acts as a modulator of quorum sensing. Res Microbiol 154:207–213

Ledgham F, Ventre I, Soscia C, Foglino M, Sturgis JN, Lazdunski A (2003b) Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 48:199–210

Lee J, Wu J, Deng Y, Wang J, Wang C, Wang J, Chang C, Dong Y, Williams P, Zhang LH (2013) A cell-cell communication signal integrates quorum sensing and stress response. Nature Chem Biol 9:339–343

Lépine F, Milot S, Déziel E, He J, Rahme LG (2004) Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa. J Am Soc Mass Spectrom 15:862–869

Lequette Y, Greenberg EP (2005) Timing and localization of rhamnolipid synthesis gene expression in Pseudomonas aeruginosa biofilms. J Bacteriol 187:37–44

Li LL, Malone JE, Iglewski BH (2007) Regulation of the Pseudomonas aeruginosa quorum-sensing regulator VqsR. J Bacteriol 189:4367–4374

Lightbown JW, Jackson FL (1956) Inhibition of cytochrome systems of heart muscle and certain bacteria by the antagonists of dihydrostreptomycin: 2-alkyl-4-hydroxyquinoline N-oxides. Biochem J 63:130–137

Mattmann ME, Blackwell HE (2010) Small molecules that modulate quorum sensing and control virulence in Pseudomonas aeruginosa. J Org Chem 75:6737–6746

McEwan DL, Kirienko NV, Ausubel FM (2012) Host translational inhibition by Pseudomonas aeruginosa exotoxin A triggers an immune response in Caenorhabditis elegans. Cell Host Microbe 11:364–374

McKnight SL, Iglewski BH, Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 182:2702–2708

Nealson KH, Platt T, Hastings JW (1970) Cellular control of the synthesis and activity of the bacterial luminescent system. J Bacteriol 104:313–322

Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

Ochsner UA, Reiser J (1995) Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92:6424–6428

Ochsner UA, Wilderman PJ, Vasil AI, Vasil ML (2002) GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45:1277–1287

Oglesby AG, Farrow JM, Lee J-H, Tomaras AP, Greenberg E, Pesci EC, Vasil ML (2008) The influence of iron on Pseudomonas aeruginosa Physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283:15558–15567

Park PW, Pier GB, Preston MJ, Goldberger O, Fitzgerald ML, Bernfield M (2000) Syndecan-1 shedding is enhanced by LasA, a secreted virulence factor of Pseudomonas aeruginosa. J Biol Chem 275:3057–3064

Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215–1226

Passador L, Cook JM, Gambello MJ, Rust L, Iglewski BH (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127–1130

Pearson JP, Gray KM, Passador L, Tucker KD, Eberhard A, Iglewski BH, Greenberg EP (1994) Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA 91:197–201

Pearson JP, Passador L, Iglewski BH, Greenberg EP (1995) A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92:1490–1494

Pereira CS, Thompson JA, Xavier KB (2013) AI-2-mediated signalling in bacteria. FEMS Microbiol Rev 37:156–181

Pesci EC, Pearson JP, Seed PC, Iglewski BH (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132

Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP, Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:11229–11234

Pessi G, Haas D (2000) Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J Bacteriol 182:6940–6949

Pessi G, Williams F, Hindle Z, Heurlier K, Holden MT, Cámara M, Haas D, Williams P (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183:6676–6683

Rabin HR, Butler SM, Wohl MEB, Geller DE, Colin AA, Schidlow DV, Johnson CA, Konstan MW, Regelmann WE (2004) Pulmonary exacerbations in cystic fibrosis. Pediatr Pulmonol 37:400–406

Rahme LG, Tan M-W, Le L, Wong SM, Tompkins RG, Calderwood SB, Ausubel FM (1997) Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc Natl Acad Sci USA 94:13245–13250

Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, Lau GW, Mahajan-Miklos S, Plotnikova J, Tan MW, Tsongalis J et al (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci USA 97:8815–8821

Rampioni G, Schuster M, Greenberg EP, Bertani I, Grasso M, Venturi V, Zennaro E, Leoni L (2007) RsaL provides quorum sensing homeostasis and functions as a global regulator of gene expression in Pseudomonas aeruginosa. Mol Microbiol 66:1557–1565

Redfield RJ (2002) Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10:365–370

Reimmann C, Beyeler M, Latifi A, Winteler H, Foglino M, Lazdunski A, Haas D (1997) The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol Microbiol 24:309–319

Roy-Burman A, Savel RH, Racine S, Swanson BL, Revadigar NS, Fujimoto J, Sawa T, Frank DW, Wiener-Kronish JP (2001) Type III protein secretion is associated with death in lower respiratory and systemic Pseudomonas aeruginosa infections. J Infect Dis 183:1767–1774

Ryall B, Davies JC, Wilson R, Shoemark A, Williams HD (2008) Pseudomonas aeruginosa, cyanide accumulation and lung function in CF and non-CF bronchiectasis patients. Eur Respir J 32:740–747

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

Schaber JA, Carty NL, McDonald NA, Graham ED, Cheluvappa R, Griswold JA, Hamood AN (2004) Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa. J Med Microbiol 53:841–853

Schafhauser J, Lepine F, McKay G, Ahlgren HG, Khakimova M, Nguyen D (2014) The stringent response modulates 4-hydroxy-2-alkylquinoline biosynthesis and quorum-sensing hierarchy in Pseudomonas aeruginosa. J Bacteriol 196:1641–1650

Schertzer JW, Boulette ML, Whiteley M (2009) More than a signal: non-signaling properties of quorum sensing molecules. Trends Microbiol 17:189–195

Schuster M, Greenberg EP (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296:73–81

Schuster M, Greenberg EP (2007) Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8:287

Schuster M, Lostroh CP, Ogi T, Greenberg EP (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079

Schuster M, Urbanowski ML, Greenberg EP (2004) Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc Natl Acad Sci USA 101:15833–15839

Seet Q, Zhang LH (2011) Anti-activator QslA defines the quorum sensing threshold and response in Pseudomonas aeruginosa. Mol Microbiol 80:951–965

Siehnel R, Traxler B, An DD, Parsek MR, Schaefer AL, Singh PK (2010) A unique regulator controls the activation threshold of quorum-regulated genes in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 107:7916–7921

Sio CF, Otten LG, Cool RH, Diggle SP, Braun PG, Bos R, Daykin M, Camara M, Williams P, Quax WJ (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74:1673–1682

Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D’Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM et al (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103:8487–8492

Solomonson LP (1981) Cyanide as a metabolic inhibitor. In: Vennesland EECB, Knowles CJ, Westley J, Wissing F (eds) Cyanide in biology. Academic Press, London, pp 11–28

Stewart GS, Williams P (1992) lux genes and the applications of bacterial bioluminescence. Journal of general microbiology 138:1289–1300

Strempel N, Neidig A, Nusser M, Geffers R, Vieillard J, Lesouhaitier O, Brenner-Weiss G, Overhage J (2013) Human host defense peptide LL-37 stimulates virulence factor production and adaptive resistance in Pseudomonas aeruginosa. PLoS One 8:e82240

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

Tan TT (2008) “Future” threat of gram-negative resistance in Singapore. Ann Acad Med Singap 37:884–890

Thompson LS, Webb JS, Rice SA, Kjelleberg S (2003) The alternative sigma factor RpoN regulates the quorum sensing gene rhlI in Pseudomonas aeruginosa. FEMS Microbiol Lett 220:187–195

Toder DS, Gambello MJ, Iglewski BH (1991) Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR. Mol Microbiol 5:2003–2010

Van Delden C, Iglewski BH (1998) Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg Infect Dis 4:551–560

Van Delden C, Pesci EC, Pearson JP, Iglewski BH (1998) Starvation selection restores elastase and rhamnolipid production in a Pseudomonas aeruginosa quorum-sensing mutant. Infect Immun 66:4499–4502

van Delden C, Comte R, Bally AM (2001) Stringent response activates quorum sensing and modulates cell density-dependent gene expression in Pseudomonas aeruginosa. J Bacteriol 183:5376–5384

Ventre I, Ledgham F, Prima V, Lazdunski A, Foglino M, Sturgis JN (2003) Dimerization of the quorum sensing regulator RhlR: development of a method using EGFP fluorescence anisotropy. Mol Microbiol 48:187–198

von Bodman SB, Willey JM, Diggle SP (2008) Cell–cell communication in bacteria: united we stand. J Bacteriol 190:4377–4391

Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E, Coleman JP, Pesci EC (2005) Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa. J Bacteriol 187:4372–4380

Westblade LF, Ilag LL, Powell AK, Kolb A, Robinson CV, Busby SJ (2004) Studies of the Escherichia coli Rsd-sigma70 complex. J Mol Biol 335:685–692

Whitchurch CB, Beatson SA, Comolli JC, Jakobsen T, Sargent JL, Bertrand JJ, West J, Klausen M, Waite LL, Kang PJ et al (2005) Pseudomonas aeruginosa fimL regulates multiple virulence functions by intersecting with Vfr-modulated pathways. Mol Microbiol 55:1357–1378

Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404

Whiteley M, Greenberg EP (2001) Promoter specificity elements in Pseudomonas aeruginosa quorum-sensing-controlled genes. J Bacteriol 183:5529–5534

Whiteley M, Lee KM, Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:13904–13909

Whiteley M, Parsek MR, Greenberg EP (2000) Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J Bacteriol 182:4356–4360

Williams P, Bainton NJ, Swift S, Chhabra SR, Winson MK, Stewart GS, Salmond GP, Bycroft BW (1992) Small molecule-mediated density-dependent control of gene expression in prokaryotes: bioluminescence and the biosynthesis of carbapenem antibiotics. FEMS Microbiol Lett 100:161–167

Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GP, Bycroft BW et al (1995) Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92:9427–9431

Winzer K, Falconer C, Garber NC, Diggle SP, Camara M, Williams P (2000) The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J Bacteriol 182:6401–6411

Wolz C, Hohloch K, Ocaktan A, Poole K, Evans RW, Rochel N, Albrecht-Gary AM, Abdallah MA, Doring G (1994) Iron release from transferrin by pyoverdin and elastase from Pseudomonas aeruginosa. Infect Immun 62:4021–4027

Wu L, Estrada O, Zaborina O, Bains M, Shen L, Kohler JE, Patel N, Musch MW, Chang EB, Fu YX et al (2005) Recognition of host immune activation by Pseudomonas aeruginosa. Science 309:774–777

Xiao G, Deziel E, He J, Lepine F, Lesic B, Castonguay MH, Milot S, Tampakaki AP, Stachel SE, Rahme LG (2006a) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689–1699

Xiao G, He J, Rahme LG (2006b) Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 152:1679–1686

Yanagihara K, Tomono K, Kaneko Y, Miyazaki Y, Tsukamoto K, Hirakata Y, Mukae H, Kadota J, Murata I, Kohno S (2003) Role of elastase in a mouse model of chronic respiratory Pseudomonas aeruginosa infection that mimics diffuse panbronchiolitis. Journal of medical microbiology 52:531–535

Zaborin A, Romanowski K, Gerdes S, Holbrook C, Lepine F, Long J, Poroyko V, Diggle SP, Wilke A, Righetti K et al (2009) Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc Natl Acad Sci USA 106:6327–6332

Zaborina O, Lepine F, Xiao G, Valuckaite V, Chen Y, Li T, Ciancio M, Zaborin A, Petrof EO, Turner JR et al (2007) Dynorphin activates quorum sensing quinolone signaling in Pseudomonas aeruginosa. PLoS Pathog 3:e35

Zhang L, Murphy PJ, Kerr A, Tate ME (1993) Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones. Nature 362:446–448