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Volume 69, Issue 1

The third quorum-sensing system of : quinolone signal and the enigmatic PqsE protein Free

Abstract

is an opportunistic pathogen that produces several virulence factors such as lectin A, pyocyanin, elastase and rhamnolipids. These compounds are controlled transcriptionally by three quorum-sensing circuits, two based on the synthesis and detection of -acyl-homoserine-lactone termed the Las and Rhl system and a third system named the quinolone signal (PQS) system, which is responsible for generating 2-alkyl-4(1 h)-quinolones (AQs). The transcriptional regulator called PqsR binds to the promoter of in the presence of PQS or HHQ creating a positive feedback-loop. PqsE, encoded in the operon for AQ synthesis, is a crucial protein for pyocyanin production, activating the Rhl system by a still not fully understood mechanism. In turn, the regulation of the PQS system is modulated by Las and Rhl systems, which act positively and negatively, respectively. This review focuses on the PQS system, from its discovery to its role in pathogenesis, such as iron depletion and pyocyanin synthesis that involves the PqsE protein – an intriguing player of this system.

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  • Accepted:
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Keyword(s): 2-alkyl-4-quinolone , Pseudomonas aeruginosa , pyocyanin , quorum-sensing and virulence
© 2020 The Authors
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2020-01-01
2024-04-24
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References

  1. Nealson KH, Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system. Microbiology 1970; 104:313–322
     [Google Scholar]
  2. Luzar MA, Montie TC. Avirulence and altered physiological properties of cystic fibrosis strains of Pseudomonas aeruginosa . Infect Immun 1985; 50:572–576
     [Google Scholar]
  3. Murphy TF, Brauer AL, Eschberger K, Lobbins P, Grove L et al. Pseudomonas aeruginosa in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008; 177:853–860 [View Article]
     [Google Scholar]
  4. Pearson JP, Pesci EC, Iglewski BH. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 1997; 179:5756–5767 [View Article]
     [Google Scholar]
  5. Gambello MJ, Kaye S, Iglewski BH. Lasr of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression. Infect Immun 1993; 61:1180–1184
     [Google Scholar]
  6. Pessi G, Haas D. 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 2000; 182:6940–6949 [View Article]
     [Google Scholar]
  7. Ochsner UA, Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa . Proc Natl Acad Sci USA 1995; 92:6424–6428 [View Article]
     [Google Scholar]
  8. Medina G, Juárez K, Díaz R, Soberón-Chávez G. Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 2003; 149:3073–3081 [View Article]
     [Google Scholar]
  9. Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G et al. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 2001; 183:6454–6465 [View Article]
     [Google Scholar]
  10. Sakuragi Y, Kolter R. Quorum-Sensing regulation of the biofilm matrix genes (Pel) of Pseudomonas aeruginosa . J Bacteriol 2007; 189:5383–5386 [View Article]
     [Google Scholar]
  11. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 1996; 21:1137–1146 [View Article]
     [Google Scholar]
  12. Williams P, Winzer K, Chan WC, Cámara M. Look who's talking: communication and quorum sensing in the bacterial world. Phil Trans R Soc B 2007; 362:1119–1134 [View Article]
     [Google Scholar]
  13. Pesci EC, Pearson JP, Seed PC, Iglewski BH, Pesci EC. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa . J Bacteriol 1997; 179:3127–3132 [View Article]
     [Google Scholar]
  14. Gambello MJ, Iglewski BH. Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 1991; 173:3000–3009 [View Article]
     [Google Scholar]
  15. Pearson JP, Passador L, Iglewski BH, Greenberg EP, Barbara H. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa . Proc Natl Acad Sci USA 1995; 92:1490–1494 [View Article]
     [Google Scholar]
  16. Pearson JP, Gray KM, Passador L, Tuckert KD, Eberhard A et al. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Biochemistry 1994; 91:197–201
     [Google Scholar]
  17. Ochsner UA, Koch AK, Fiechter A, Reiser J. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa . J Bacteriol 1994; 176:2044–2054 [View Article]
     [Google Scholar]
  18. Pesci EC, Milbank JBJ, Pearson JP, McKnight S, Kende AS et al. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 1999; 96:11229–11234 [View Article]
     [Google Scholar]
  19. Cao H, Krishnan G, Goumnerov B, Tsongalis J, Tompkins R et al. 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 2001; 98:14613–14618 [View Article]
     [Google Scholar]
  20. Xiao G, Déziel E, He J, Lépine F, Lesic B et al. MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 2006; 62:1689–1699 [View Article]
     [Google Scholar]
  21. Wade DS, Calfee MW, Rocha ER, Ling EA, Engstrom E et al. Regulation of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa . J Bacteriol 2005; 187:4372–4380 [View Article]
     [Google Scholar]
  22. Mukherjee S, Moustafa D, Smith CD, Goldberg JB, Bassler BL. The RhlR quorum-sensing receptor controls Pseudomonas aeruginosa pathogenesis and biofilm development independently of its canonical homoserine lactone autoinducer. PLoS Pathog 2017; 13:e1006504–1006525 [View Article]
     [Google Scholar]
  23. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 2003; 185:2080–2095 [View Article]
     [Google Scholar]
  24. Schuster M, Lostroh CP, Ogi T, Greenberg EP, Identification GEP. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 2003; 185:2066–2079 [View Article]
     [Google Scholar]
  25. Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR et al. The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 2007; 14:87–96 [View Article]
     [Google Scholar]
  26. Maura D, Hazan R, Kitao T, Ballok AE, Rahme LG. Evidence for direct control of virulence and defense gene circuits by the Pseudomonas aeruginosa quorum sensing regulator, MvfR. Sci Rep 2016; 6:1–14 [View Article]
     [Google Scholar]
  27. Déziel E, Lépine F, Milot S, He J, Mindrinos MN et al. 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 2004; 101:1339–1344 [View Article]
     [Google Scholar]
  28. Lépine F, Milot S, Déziel E, He J, Rahme LG. Electrospray/mass spectrometric identification and analysis of 4-hydroxy-2-alkylquinolines (HAQs) produced by Pseudomonas aeruginosa . J Am Soc Mass Spectrom 2004; 15:862–869 [View Article]
     [Google Scholar]
  29. Singh G, Wu B, Baek MS, Camargo A, Nguyen A et al. Secretion of Pseudomonas aeruginosa type III cytotoxins is dependent on pseudomonas quinolone signal concentration. Microb Pathog 2010; 49:196–203 [View Article]
     [Google Scholar]
  30. Rampioni G, Falcone M, Heeb S, Frangipani E, Fletcher MP et al. Unravelling the Genome-Wide Contributions of Specific 2-Alkyl-4-Quinolones and PqsE to Quorum Sensing in Pseudomonas aeruginosa . PLoS Pathog 2016; 12:e1006029 [View Article]
     [Google Scholar]
  31. Calfee MW, Coleman JP, Pesci EC. Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2001; 98:11633–11637 [View Article]
     [Google Scholar]
  32. Zhang Y-M, Frank MW, Zhu K, Mayasundari A, Rock CO. Pqsd is responsible for the synthesis of 2,4-dihydroxyquinoline, an extracellular metabolite produced by Pseudomonas aeruginosa . J Biol Chem 2008; 283:28788–28794 [View Article]
     [Google Scholar]
  33. Coleman JP, Hudson LL, McKnight SL, Farrow JM, Calfee MW et al. Pseudomonas aeruginosa PqsA is an anthranilate-coenzyme A ligase. J Bacteriol 2008; 190:1247–1255 [View Article]
     [Google Scholar]
  34. Schertzer JW, Brown SA, Whiteley M. Oxygen levels rapidly modulate Pseudomonas aeruginosa social behaviours via substrate limitation of PqsH. Mol Microbiol 2010; 77:1527–1538 [View Article]
     [Google Scholar]
  35. Dulcey CE, Dekimpe V, Fauvelle DA, Milot S, Groleau MC et al. The end of an old hypothesis: the Pseudomonas signaling molecules 4-hydroxy-2-alkylquinolines derive from fatty acids, not 3-ketofatty acids. Chem Biol 2013; 20:1481–1491 [View Article]
     [Google Scholar]
  36. Hennecke U, Fetzner S, Drees SL, Belviso BD, Ernst S et al. PqsL uses reduced flavin to produce 2-hydroxylaminobenzoylacetate, a preferred PqsBC substrate in alkyl quinolone biosynthesis in Pseudomonas aeruginosa . J Biol Chem 2018; 293:9345–9357
     [Google Scholar]
  37. Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa . J Bacteriol 2002; 184:6472–6480 [View Article]
     [Google Scholar]
  38. Dötsch A, Eckweiler D, Schniederjans M, Zimmermann A, Jensen V, Scharfe M et al. The Pseudomonas aeruginosa transcriptome in planktonic cultures and static biofilms using RNA sequencing. PLoS One 2012; 7:e31092 [View Article]
     [Google Scholar]
  39. Xiao G, He J, Rahme LG. Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 2006; 152:1679–1686 [View Article]
     [Google Scholar]
  40. Brouwer S, Pustelny C, Ritter C, Klinkert B, Narberhaus F et al. The PqsR and RhlR transcriptional regulators determine the level of Pseudomonas quinolone signal synthesis in Pseudomonas aeruginosa by producing two different pqsABCDE mRNA isoforms. J Bacteriol 2014; 196:4163–4171 [View Article]
     [Google Scholar]
  41. Kang H, Gan J, Zhao J, Kong W, Zhang J et al. Crystal structure of Pseudomonas aeruginosa RsaL bound to promoter DNA reaffirms its role as a global regulator involved in quorum-sensing. Nucleic Acids Res 2017; 45:699–710 [View Article]
     [Google Scholar]
  42. Rampioni G, Bertani I, Zennaro E, Polticelli F, Venturi V et al. The quorum-sensing negative regulator RsaL of Pseudomonas aeruginosa binds to the lasI promoter. J Bacteriol 2006; 188:815–819 [View Article]
     [Google Scholar]
  43. Farrow JM, Pesci EC. Distal and proximal promoters co-regulate pqsR expression in Pseudomonas aeruginosa . Mol Microbiol 2017; 104:78–91 [View Article]
     [Google Scholar]
  44. Farrow JM, Hudson LL, Wells G, Coleman JP, Pesci EC. CysB Negatively Affects the Transcription of pqsR and Pseudomonas Quinolone Signal Production in Pseudomonas aeruginosa . J Bacteriol 2015; 197:1988–2002 [View Article]
     [Google Scholar]
  45. Liang H, Li L, Dong Z, Surette MG, Duan K. The YebC family protein PA0964 negatively regulates the Pseudomonas aeruginosa quinolone signal system and pyocyanin production. J Bacteriol 2008; 190:6217–6227 [View Article]
     [Google Scholar]
  46. Sonnleitner E, Gonzalez N, Sorger-Domenigg T, Heeb S, Richter AS et al. The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol Microbiol 2011; 80:868–885 [View Article]
     [Google Scholar]
  47. Jensen V, Löns D, Zaoui C, Bredenbruch F, Meissner A et al. RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J Bacteriol 2006; 188:8601–8606 [View Article]
     [Google Scholar]
  48. Zhang L, Gao Q, Chen W, Qin H, Hengzhuang W et al. Regulation of pqs quorum sensing via catabolite repression control in Pseudomonas aeruginosa . Microbiology 2013; 159:1931–1936 [View Article]
     [Google Scholar]
  49. Apidianakis Y, Astrakas C, De E. Homeostatic interplay between bacterial cell-cell signaling and iron in virulence. PLoS Pathog 2010; 6:1–14
     [Google Scholar]
  50. Rampioni G, Pustelny C, Fletcher MP, Wright VJ, Bruce M et al. Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts. Environ Microbiol 2010; 12:1659–1673 [View Article]
     [Google Scholar]
  51. Wells G, Palethorpe S, Pesci EC. PsrA controls the synthesis of the Pseudomonas aeruginosa quinolone signal via repression of the fade homolog, PA0506. PLoS One 2017; 12:e0189331 [View Article]
     [Google Scholar]
  52. Hall S, McDermott C, Anoopkumar-Dukie S, McFarland A, Forbes A et al. Cellular effects of pyocyanin, a secreted virulence factor of Pseudomonas aeruginosa . Toxins 2016; 8:236–14 [View Article]
     [Google Scholar]
  53. Rada B, Lekstrom K, Damian S, Dupuy C, Leto TL et al. The Pseudomonas toxin pyocyanin inhibits the dual oxidase-based antimicrobial system as it imposes oxidative stress on airway epithelial cells. J Immunol 2008; 181:4883–4893 [View Article]
     [Google Scholar]
  54. Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin Microbiol Rev 2002; 15:194–222 [View Article]
     [Google Scholar]
  55. Lau GW, Hassett DJ, Ran H, Kong F. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 2004; 10:599–606 [View Article]
     [Google Scholar]
  56. Whiteley M, Greenberg EP. Promoter Specificity Elements in Pseudomonas aeruginosa Quorum-Sensing-Controlled Genes. J Bacteriol 2001; 183:5529–5534 [View Article]
     [Google Scholar]
  57. Brint JM, Ohman DE. 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. J Bacteriol 1995; 177:7155–7163 [View Article]
     [Google Scholar]
  58. Yu S, Jensen V, Seeliger J, Feldmann I, Weber S et al. Structure elucidation and preliminary assessment of hydrolase activity of PqsE, the Pseudomonas quinolone signal (PQS) response protein. Biochemistry 2009; 48:10298–10307 [View Article]
     [Google Scholar]
  59. Zender M, Witzgall F, Drees SL, Weidel E, Maurer CK et al. Dissecting the multiple roles of PqsE in Pseudomonas aeruginosa virulence by discovery of small tool compounds. ACS Chem Biol 2016; 11:1755–1763 [View Article]
     [Google Scholar]
  60. Drees SL, Fetzner S, Drees SL, Fetzner S. PqsE of Pseudomonas aeruginosa acts as pathway-specific thioesterase in the biosynthesis of Alkylquinolone signaling molecules. Chem Biol 2015; 22:611–618 [View Article]
     [Google Scholar]
  61. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Cámara M et al. 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 2003; 50:29–43 [View Article]
     [Google Scholar]
  62. McKnight SL, Iglewski BH, Pesci EC. The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa . J Bacteriol 2000; 182:2702–2708 [View Article]
     [Google Scholar]
  63. Recinos DA, Sekedat MD, Hernandez A, Cohen TS, Sakhtah H et al. Redundant phenazine operons in Pseudomonas aeruginosa exhibit environment-dependent expression and differential roles in pathogenicity. Proc Natl Acad Sci USA 2012; 109:19420–19425 [View Article]
     [Google Scholar]
  64. Mukherjee S, Moustafa DA, Stergioula V, Smith CD, Goldberg JB et al. The PqsE and RhlR proteins are an autoinducer synthase-receptor pair that control virulence and biofilm development in Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2018; 115:E9411–E9418 [View Article]
     [Google Scholar]
  65. Bleves S, Soscia C, Nogueira-Orlandi P, Lazdunski A, Filloux A. Quorum sensing negatively controls type III secretion regulon expression in Pseudomonas aeruginosa PAO1. J Bacteriol 2005; 187:3898–3902 [View Article]
     [Google Scholar]
  66. Farrow JM, Sund ZM, Ellison ML, Wade DS, Coleman JP et al. Pqse functions independently of PqsR-Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 2008; 190:7043–7051 [View Article]
     [Google Scholar]
  67. Liu YC, Hussain F, Negm O, Paiva AC, Halliday N et al. Contribution of the Alkylquinolone Quorum-Sensing System to the Interaction of Pseudomonas aeruginosa With Bronchial Epithelial Cells. Front Microbiol 2018; 9:1–12 [View Article]
     [Google Scholar]
  68. Lazdunski A, Guzzo J, Filloux A, Bally M, Murgier M. Secretion of extracellular proteins by Pseudomonas aeruginosa . Biochimie 1990; 72:147–156 [View Article]
     [Google Scholar]
  69. Kuang Z, Hao Y, Walling BE, Jeffries JL, Ohman DE et al. Pseudomonas aeruginosa elastase provides an escape from phagocytosis by degrading the pulmonary surfactant protein-A. PLoS One 2011; 6:e27091 [View Article]
     [Google Scholar]
  70. Soares MP, Weiss G. The iron age of host–microbe interactions. EMBO Rep 2015; 16:1482–1500 [View Article]
     [Google Scholar]
  71. Cornelis P, Dingemans J. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections. Front Cell Infect Microbiol 2013; 3:1–7 [View Article]
     [Google Scholar]
  72. Bredenbruch F, Geffers R, Nimtz M, Buer J, Häussler S. The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 2006; 8:1318–1329 [View Article]
     [Google Scholar]
  73. Cheng J, Qian PY, Zhang W, Wang Y, Yang X et al. A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nat Commun 2017; 8:1–12
     [Google Scholar]
  74. Troxell B, Hassan HM. Transcriptional regulation by ferric uptake regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 2013; 3:1–13 [View Article]
     [Google Scholar]
  75. Gruber JD, Chen W, Parnham S, Beauchesne K, Moeller P et al. The role of 2,4-dihydroxyquinoline (DHQ) in Pseudomonas aeruginosa pathogenicity. PeerJ 2016; 4:e1495 [View Article]
     [Google Scholar]
  76. Kesarwani M, Hazan R, He J, Que Y, Apidianakis Y et al. Correction: a quorum sensing regulated small volatile molecule reduces acute virulence and promotes chronic infection phenotypes. PLoS Pathog 2011; 7:1–12 [View Article]
     [Google Scholar]
  77. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 2002; 109:317–325 [View Article]
     [Google Scholar]
  78. Schobert M, Jahn D. Anaerobic physiology of Pseudomonas aeruginosa in the cystic fibrosis lung. Int J Med Microbiol 2010; 300:549–556 [View Article]
     [Google Scholar]
  79. Hooi DSW, Bycroft BW, Chhabra SR, Williams P, Pritchard DI. Differential Immune Modulatory Activity of Pseudomonas aeruginosa Quorum-Sensing Signal Molecules. Infect Immun 2004; 72:6463–6470 [View Article]
     [Google Scholar]
  80. Skindersoe ME, Zeuthen LH, Brix S, Fink LN, Lazenby J et al. Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. FEMS Immunol Med Microbiol 2009; 55:335–345 [View Article]
     [Google Scholar]
  81. Kim K, Kim SH, Lépine F, Cho YH, Lee GR. Global gene expression analysis on the target genes of PQS and HHQ in J774A.1 monocyte/macrophage cells. Microb Pathog 2010; 49:174–180 [View Article]
     [Google Scholar]
  82. Kim K, Kim YU, Koh BH, Hwang SS, Kim SH et al. HHQ and PQS, two Pseudomonas aeruginosa quorum-sensing molecules, down-regulate the innate immune responses through the nuclear factor-κB pathway. Immunology 2010; 129:578–588 [View Article]
     [Google Scholar]
  83. Ha DG, Merritt JH, Hampton TH, Hodgkinson JT, Janecek M et al. 2-Heptyl-4-quinolone, a precursor of the Pseudomonas quinolone signal molecule, modulates swarming motility in Pseudomonas aeruginosa . J Bacteriol 2011; 193:6770–6780 [View Article]
     [Google Scholar]
  84. Alcalde-Rico M, Olivares-Pacheco J, Alvarez-Ortega C, Cámara M, Martínez JL. Role of the multidrug resistance efflux pump MexCD-OprJ in the Pseudomonas aeruginosa quorum sensing response. Front Microbiol 2018; 9:1–16 [View Article]
     [Google Scholar]
  85. Fetar H, Gilmour C, Klinoski R, Daigle DM, Dean CR et al. mexEF-oprN multidrug efflux operon of Pseudomonas aeruginosa: regulation by the MexT activator in response to nitrosative stress and chloramphenicol. Antimicrob Agents Chemother 2011; 55:508–514 [View Article]
     [Google Scholar]
  86. Lamarche MG, Déziel E. MexEF-OprN efflux pump exports the Pseudomonas quinolone signal (PQS) precursor HHQ (4-hydroxy-2-heptylquinoline). PLoS One 2011; 6:e24310–24312 [View Article]
     [Google Scholar]
  87. Cox CD, Parker J. Use of 2-Aminoacetophenone Production in Identification of Pseudomonas aeruginosa ; 1979; 9479–484
  88. Que YA, Hazan R, Strobel B, Maura D, He J et al. A quorum sensing small volatile molecule promotes antibiotic tolerance in bacteria. PLoS One 2013; 8:e80140 [View Article]
     [Google Scholar]
  89. Hoffman LR, Déziel E, D'Argenio DA, Lépine F, Emerson J et al. Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa . Proc Natl Acad Sci USA 2006; 103:19890–19895 [View Article]
     [Google Scholar]
  90. Hazan R, Que YA, Maura D, Strobel B, Majcherczyk PA et al. Auto poisoning of the respiratory chain by a Quorum-Sensing-Regulated molecule favors biofilm formation and antibiotic tolerance. Curr Biol 2016; 26:195–206 [View Article]
     [Google Scholar]
  91. Diggle SP, Lumjiaktase P, Dipilato F, Winzer K, Kunakorn M et al. Functional genetic analysis reveals a 2-Alkyl-4-quinolone signaling system in the human pathogen Burkholderia pseudomallei and related bacteria. Chem Biol 2006; 13:701–710 [View Article]
     [Google Scholar]
  92. Vial L, Lépine F, Milot S, Groleau MC, Dekimpe V et al. Burkholderia pseudomallei, B. thailandensis, and B. ambifaria produce 4-hydroxy-2-alkylquinoline analogues with a methyl group at the 3 position that is required for quorum-sensing regulation. J Bacteriol 2008; 190:5339–5352 [View Article]
     [Google Scholar]
  93. Elbourne L, Tremblay S, Ren Q, Roy PH, Tetu SG. Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS One 2010; 5:1–10
     [Google Scholar]
  94. Grosso-Becerra MV, González-Valdez A, Granados-Martínez MJ, Morales E, Servín-González L et al. Pseudomonas aeruginosa ATCC 9027 is a non-virulent strain suitable for mono-rhamnolipids production. Appl Microbiol Biotechnol 2016; 100:9995–10004 [View Article]
     [Google Scholar]
  95. Grosso-Becerra M-V, Santos-Medellín C, González-Valdez A, Méndez J-L, Delgado G et al. Pseudomonas aeruginosa clinical and environmental isolates constitute a single population with high phenotypic diversity. BMC Genomics 2014; 15:318–14 [View Article]
     [Google Scholar]
  96. Morales E, González-Valdez A, Servín-González L, Soberón-Chávez G. Pseudomonas aeruginosa quorum-sensing response in the absence of functional LasR and LasI proteins: the case of strain 148, a virulent dolphin isolate. FEMS Microbiol Lett 2017; 364:1–10 [View Article]
     [Google Scholar]
  97. Maura D, Rahme LG. Pharmacological inhibition of the formation and potentiates Antibiotic- mediated biofilm disruption. Antimicrob Agents Chemother 2017; 61:15–17
     [Google Scholar]
  98. Soukarieh F, Vico Oton E, Dubern J-F, Gomes J, Halliday N et al. In silico and in vitro-guided identification of inhibitors of alkylquinolone-dependent quorum sensing in Pseudomonas aeruginosa . Molecules 2018; 23:257–15 [View Article]
     [Google Scholar]
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The third quorum-sensing system of Pseudomonas aeruginosa: Pseudomonas quinolone signal and the enigmatic PqsE protein
J. Med. Microbiol. 69, 25 (2020); https://doi.org/10.1099/jmm.0.001116
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