1887

Abstract

Bacteria communicate through the production of diffusible signal molecules termed autoinducers. The molecules are produced at basal levels and accumulate during growth. Once a critical concentration has been reached, autoinducers can activate or repress a number of target genes. Because the control of gene expression by autoinducers is cell-density-dependent, this phenomenon has been called quorum sensing. Quorum sensing controls virulence gene expression in numerous micro-organisms. In some cases, this phenomenon has proven relevant for bacterial virulence . In this article, we provide a few examples to illustrate how quorum sensing can act to control bacterial virulence in a multitude of ways. Several classes of autoinducers have been described to date and we present examples of how each of the major types of autoinducer can be involved in bacterial virulence. As quorum sensing controls virulence, it has been considered an attractive target for the development of new therapeutic strategies. We discuss some of the new strategies to combat bacterial virulence based on the inhibition of bacterial quorum sensing systems.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.038794-0
2010-08-01
2024-12-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/8/2271.html?itemId=/content/journal/micro/10.1099/mic.0.038794-0&mimeType=html&fmt=ahah

References

  1. Abdelnour A., Arvidson S., Bremell T., Ryden C., Tarkowski A. 1993; The accessory gene regulator ( agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect Immun 61:3879–3885
    [Google Scholar]
  2. Antunes L. C., Ferreira R. B. 2009; Intercellular communication in bacteria. Crit Rev Microbiol 35:69–80
    [Google Scholar]
  3. Antunes L. C., Schaefer A. L., Ferreira R. B., Qin N., Stevens A. M., Ruby E. G., Greenberg E. P. 2007; Transcriptome analysis of the Vibrio fischeri LuxR–LuxI regulon. J Bacteriol 189:8387–8391
    [Google Scholar]
  4. Asaduzzaman S. M., Sonomoto K. 2009; Lantibiotics: diverse activities and unique modes of action. J Biosci Bioeng 107:475–487
    [Google Scholar]
  5. Balaban N., Novick R. P. 1995; Translation of RNAIII, the Staphylococcus aureus agr regulatory RNA molecule, can be activated by a 3′-end deletion. FEMS Microbiol Lett 133:155–161
    [Google Scholar]
  6. Balaban N., Cirioni O., Giacometti A., Ghiselli R., Braunstein J. B., Silvestri C., Mocchegiani F., Saba V., Scalise G. 2007; Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob Agents Chemother 51:2226–2229
    [Google Scholar]
  7. Bassler B. L., Losick R. 2006; Bacterially speaking. Cell 125:237–246
    [Google Scholar]
  8. Bassler B. L., Wright M., Showalter R. E., Silverman M. R. 1993; Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 9:773–786
    [Google Scholar]
  9. Bendiak G. N., Ratjen F. 2009; The approach to Pseudomonas aeruginosa in cystic fibrosis. Semin Respir Crit Care Med 30:587–595
    [Google Scholar]
  10. Benito Y., Kolb F. A., Romby P., Lina G., Etienne J., Vandenesch F. 2000; Probing the structure of RNAIII, the Staphylococcus aureus agr regulatory RNA, and identification of the RNA domain involved in repression of protein A expression. RNA 6:668–679
    [Google Scholar]
  11. Bodey G. P., Bolivar R., Fainstein V., Jadeja L. 1983; Infections caused by Pseudomonas aeruginosa. Rev Infect Dis 5:279–313
    [Google Scholar]
  12. Booth M. C., Cheung A. L., Hatter K. L., Jett B. D., Callegan M. C., Gilmore M. S. 1997; Staphylococcal accessory regulator ( sar) in conjunction with agr contributes to Staphylococcus aureus virulence in endophthalmitis. Infect Immun 65:1550–1556
    [Google Scholar]
  13. Bowden M. G., Chen W., Singvall J., Xu Y., Peacock S. J., Valtulina V., Speziale P., Hook M. 2005; Identification and preliminary characterization of cell-wall-anchored proteins of Staphylococcus epidermidis. Microbiology 151:1453–1464
    [Google Scholar]
  14. Bredenbruch F., Geffers R., Nimtz M., Buer J., Häussler S. 2006; The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 8:1318–1329
    [Google Scholar]
  15. Cao H., Krishnan G., Goumnerov B., Tsongalis J., Tompkins R., Rahme L. G. 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 U S A 98:14613–14618
    [Google Scholar]
  16. Celli J., Deng W., Finlay B. B. 2000; Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell Microbiol 2:1–9
    [Google Scholar]
  17. Cheung A. L., Eberhardt K. J., Chung E., Yeaman M. R., Sullam P. M., Ramos M., Bayer A. S. 1994; Diminished virulence of a sar−/ agr− mutant of Staphylococcus aureus in the rabbit model of endocarditis. J Clin Invest 94:1815–1822
    [Google Scholar]
  18. Chugani S. A., Whiteley M., Lee K. M., D'Argenio D., Manoil C., Greenberg E. P. 2001; QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 98:2752–2757
    [Google Scholar]
  19. Cirioni O., Ghiselli R., Minardi D., Orlando F., Mocchegiani F., Silvestri C., Muzzonigro G., Saba V., Scalise G. other authors 2007; RNAIII-inhibiting peptide affects biofilm formation in a rat model of staphylococcal ureteral stent infection. Antimicrob Agents Chemother 51:4518–4520
    [Google Scholar]
  20. Clarke M. B., Hughes D. T., Zhu C., Boedeker E. C., Sperandio V. 2006; The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci U S A 103:10420–10425
    [Google Scholar]
  21. Collier D. N., Anderson L., McKnight S. L., Noah T. L., Knowles M., Boucher R., Schwab U., Gilligan P., Pesci E. C. 2002; A bacterial cell to cell signal in the lungs of cystic fibrosis patients. FEMS Microbiol Lett 215:41–46
    [Google Scholar]
  22. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298
    [Google Scholar]
  23. De Kievit T. R., Iglewski B. H. 2000; Bacterial quorum sensing in pathogenic relationships. Infect Immun 68:4839–4849
    [Google Scholar]
  24. De Kievit T. R., Gillis R., Marx S., Brown C., Iglewski B. H. 2001; Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67:1865–1873
    [Google Scholar]
  25. Dekimpe V., Déziel E. 2009; Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712–723
    [Google Scholar]
  26. DeLisa M. P., Wu C. F., Wang L., Valdes J. J., Bentley W. E. 2001; DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 183:5239–5247
    [Google Scholar]
  27. Déziel E., Lépine F., Milot S., He J., Mindrinos M. N., Tompkins R. G., Rahme L. G. 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 U S A 101:1339–1344
    [Google Scholar]
  28. Déziel E., Gopalan S., Tampakaki A. P., Lepine F., Padfield K. E., Saucier M., Xiao G., Rahme L. G. 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
    [Google Scholar]
  29. Diggle S. P., Cornelis P., Williams P., Camara M. 2006; 4-Quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 296:83–91
    [Google Scholar]
  30. Diggle S. P., Gardner A., West S. A., Griffin A. S. 2007a; Evolutionary theory of bacterial quorum sensing: when is a signal not a signal?. Philos Trans R Soc Lond B Biol Sci 362:1241–1249
    [Google Scholar]
  31. Diggle S. P., Matthijs S., Wright V. J., Fletcher M. P., Chhabra S. R., Lamont I. L., Kong X., Hider R. C., Cornelis P. & other authors (2007b). The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14:87–96
    [Google Scholar]
  32. DiMango E., Zar H. J., Bryan R., Prince A. 1995; Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. J Clin Invest 96:2204–2210
    [Google Scholar]
  33. Driscoll J. A., Brody S. L., Kollef M. H. 2007; The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 67:351–368
    [Google Scholar]
  34. Eberhard A., Burlingame A. L., Eberhard C., Kenyon G. L., Nealson K. H., Oppenheimer N. J. 1981; Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449
    [Google Scholar]
  35. Engebrecht J., Silverman M. 1984; Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci U S A 81:4154–4158
    [Google Scholar]
  36. Engebrecht J., Nealson K., Silverman M. 1983; Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell 32:773–781
    [Google Scholar]
  37. Erickson D. L., Endersby R., Kirkham A., Stuber K., Vollman D. D., Rabin H. R., Mitchell I., Storey D. G. 2002; Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun 70:1783–1790
    [Google Scholar]
  38. Farrow J. M. III, Sund Z. M., Ellison M. L., Wade D. S., Coleman J. P., Pesci E. C. 2008; PqsE functions independently of PqsR– Pseudomonas quinolone signal and enhances the rhl quorum-sensing system. J Bacteriol 190:7043–7051
    [Google Scholar]
  39. Fleming V., Feil E., Sewell A. K., Day N., Buckling A., Massey R. C. 2006; Agric interference between clinical Staphylococcus aureus strains in an insect model of virulence. J Bacteriol 188:7686–7688
    [Google Scholar]
  40. Fujii T., Kadota J., Kawakami K., Iida K., Shirai R., Kaseda M., Kawamoto S., Kohno S. 1995; Long term effect of erythromycin therapy in patients with chronic Pseudomonas aeruginosa infection. Thorax 50:1246–1252
    [Google Scholar]
  41. Fuqua C. 2006; The QscR quorum-sensing regulon of Pseudomonas aeruginosa: an orphan claims its identity. J Bacteriol 188:3169–3171
    [Google Scholar]
  42. Fuqua C., Greenberg E. P. 2002; Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695
    [Google Scholar]
  43. Fuqua W. C., Winans S. C., Greenberg E. P. 1994; Quorum sensing in bacteria: the LuxR–LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275
    [Google Scholar]
  44. 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
    [Google Scholar]
  45. Gallagher L. A., McKnight S. L., Kuznetsova M. S., Pesci E. C., Manoil C. 2002; Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472–6480
    [Google Scholar]
  46. George E. A., Muir T. W. 2007; Molecular mechanisms of agr quorum sensing in virulent staphylococci. ChemBioChem 8:847–855
    [Google Scholar]
  47. Gillaspy A. F., Hickmon S. G., Skinner R. A., Thomas J. R., Nelson C. L., Smeltzer M. S. 1995; Role of the accessory gene regulator ( agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun 63:3373–3380
    [Google Scholar]
  48. Givskov M., de Nys R., Manefield M., Gram L., Maximilien R., Eberl L., Molin S., Steinberg P. D., Kjelleberg S. 1996; Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178:6618–6622
    [Google Scholar]
  49. Goerke C., Kraning K., Stern M., Doring G., Botzenhart K., Wolz C. 2000; Molecular epidemiology of community-acquired Staphylococcus aureus in families with and without cystic fibrosis patients. J Infect Dis 181:984–989
    [Google Scholar]
  50. Goh E. B., Yim G., Tsui W., McClure J., Surette M. G., Davies J. 2002; Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc Natl Acad Sci U S A 99:17025–17030
    [Google Scholar]
  51. Hazan R., He J., Xiao G., Dekimpe V., Apidianakis Y., Lesic B., Astrakas C., Déziel E., Lépine F., Rahme L. G. 2010; Homeostatic interplay between bacterial cell–cell signaling and iron in virulence. PLoS Pathog 6:e1000810
    [Google Scholar]
  52. Heurlier K., Denervaud V., Haas D. 2006; Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296:93–102
    [Google Scholar]
  53. Heyer G., Saba S., Adamo R., Rush W., Soong G., Cheung A., Prince A. 2002; Staphylococcus aureus agr and sarA functions are required for invasive infection but not inflammatory responses in the lung. Infect Immun 70:127–133
    [Google Scholar]
  54. Imamura Y., Yanagihara K., Mizuta Y., Seki M., Ohno H., Higashiyama Y., Miyazaki Y., Tsukamoto K., Hirakata Y. other authors 2004; Azithromycin inhibits MUC5AC production induced by the Pseudomonas aeruginosa autoinducer N-(3-oxododecanoyl) homoserine lactone in NCI-H292 cells. Antimicrob Agents Chemother 48:3457–3461
    [Google Scholar]
  55. Jarraud S., Lyon G. J., Figueiredo A. M., Gerard L., Vandenesch F., Etienne J., Muir T. W., Novick R. P. 2000; Exfoliatin-producing strains define a fourth agr specificity group in Staphylococcus aureus. J Bacteriol 182:6517–6522
    [Google Scholar]
  56. Jarraud S., Mougel C., Thioulouse J., Lina G., Meugnier H., Forey F., Nesme X., Etienne J., Vandenesch F. 2002; Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 70:631–641
    [Google Scholar]
  57. Ji G., Beavis R. C., Novick R. P. 1995; Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc Natl Acad Sci U S A 92:12055–12059
    [Google Scholar]
  58. Ji G., Beavis R., Novick R. P. 1997; Bacterial interference caused by autoinducing peptide variants. Science 276:2027–2030
    [Google Scholar]
  59. Karatuna O., Yagci A. 2010; Analysis of the quorum sensing-dependent virulence factor production and its relationship with antimicrobial susceptibility in Pseudomonas aeruginosa respiratory isolates. Clin Microbiol Infect
    [Google Scholar]
  60. Kehinde E. O., Rotimi V. O., Al-Hunayan A., Abdul-Halim H., Boland F., Al-Awadi K. A. 2004; Bacteriology of urinary tract infection associated with indwelling J ureteral stents. J Endourol 18:891–896
    [Google Scholar]
  61. Kielian T., Cheung A., Hickey W. F. 2001; Diminished virulence of an α-toxin mutant of Staphylococcus aureus in experimental brain abscesses. Infect Immun 69:6902–6911
    [Google Scholar]
  62. Kim C., Kim J., Park H. Y., Park H. J., Lee J. H., Kim C. K., Yoon J. 2008; Furanone derivatives as quorum-sensing antagonists of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 80:37–47
    [Google Scholar]
  63. Kim C., Kim J., Park H. Y., Lee J. H., Park H. J., Kim C. K., Yoon J. 2009a; Structural understanding of quorum-sensing inhibitors by molecular modeling study in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 83:1095–1103
    [Google Scholar]
  64. Kim K., Kim Y. U., Koh B. H., Hwang S. S., Kim S. H., Lepine F., Cho Y. H., Lee G. R. 2009b; HHQ and PQS, two Pseudomonas aeruginosa quorum-sensing molecules, down-regulate the innate immune responses through the nuclear factor- κB pathway. Immunology 129:578–588
    [Google Scholar]
  65. Kleerebezem M. 2004; Quorum sensing control of lantibiotic production; nisin and subtilin autoregulate their own biosynthesis. Peptides 25:1405–1414
    [Google Scholar]
  66. Koch C., Hoiby N. 1993; Pathogenesis of cystic fibrosis. Lancet 341:1065–1069
    [Google Scholar]
  67. Koenig R. L., Ray J. L., Maleki S. J., Smeltzer M. S., Hurlburt B. K. 2004; Staphylococcus aureus AgrA binding to the RNAIII- agr regulatory region. J Bacteriol 186:7549–7555
    [Google Scholar]
  68. Kohler T., Buckling A., van Delden C. 2009; Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sci U S A 106:6339–6344
    [Google Scholar]
  69. Kong K. F., Vuong C., Otto M. 2006; Staphylococcus quorum sensing in biofilm formation and infection. Int J Med Microbiol 296:133–139
    [Google Scholar]
  70. Kravchenko V. V., Kaufmann G. F., Mathison J. C., Scott D. A., Katz A. Z., Grauer D. C., Lehmann M., Meijler M. M., Janda K. D., Ulevitch R. J. 2008; Modulation of gene expression via disruption of NF- κB signaling by a bacterial small molecule. Science 321:259–263
    [Google Scholar]
  71. Kuipers O. P., Beerthuyzen M. M., de Ruyter P. G., Luesink E. J., de Vos W. M. 1995; Autoregulation of nisin biosynthesis in Lactococcus lactis by signal transduction. J Biol Chem 270:27299–27304
    [Google Scholar]
  72. 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
    [Google Scholar]
  73. Lauderdale K. J., Boles B. R., Cheung A. L., Horswill A. R. 2009; Interconnections between Sigma B, agr, and proteolytic activity in Staphylococcus aureus biofilm maturation. Infect Immun 77:1623–1635
    [Google Scholar]
  74. Le Berre R., Nguyen S., Nowak E., Kipnis E., Pierre M., Ader F., Courcol R., Guery B. P., Faure K. 2008; Quorum-sensing activity and related virulence factor expression in clinically pathogenic isolates of Pseudomonas aeruginosa. Clin Microbiol Infect 14:337–343
    [Google Scholar]
  75. Lepine F., Milot S., Déziel E., He J., Rahme L. G. 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
    [Google Scholar]
  76. Lina G., Jarraud S., Ji G., Greenland T., Pedraza A., Etienne J., Novick R. P., Vandenesch F. 1998; Transmembrane topology and histidine protein kinase activity of AgrC, the agr signal receptor in Staphylococcus aureus. Mol Microbiol 28:655–662
    [Google Scholar]
  77. Liu H. B., Lee J. H., Kim J. S., Park S. 2010; Inhibitors of the Pseudomonas aeruginosa quorum-sensing regulator, QscR. Biotechnol Bioeng 106:119–126
    [Google Scholar]
  78. Lyczak J. B., Cannon C. L., Pier G. B. 2000; Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2:1051–1060
    [Google Scholar]
  79. Lyon G. J., Novick R. P. 2004; Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria. Peptides 25:1389–1403
    [Google Scholar]
  80. Massey R. C., Horsburgh M. J., Lina G., Hook M., Recker M. 2006; The evolution and maintenance of virulence in Staphylococcus aureus: a role for host-to-host transmission. Nat Rev Microbiol 4:953–958
    [Google Scholar]
  81. Mayville P., Ji G., Beavis R., Yang H., Goger M., Novick R. P., Muir T. W. 1999; Structure–activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc Natl Acad Sci U S A 96:1218–1223
    [Google Scholar]
  82. McGrath S., Wade D. S., Pesci E. C. 2004; Dueling quorum sensing systems in Pseudomonas aeruginosa control the production of the Pseudomonas quinolone signal (PQS. FEMS Microbiol Lett 230:27–34
    [Google Scholar]
  83. Miller S. T., Xavier K. B., Campagna S. R., Taga M. E., Semmelhack M. F., Bassler B. L., Hughson F. M. 2004; Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol Cell 15:677–687
    [Google Scholar]
  84. Molinari G., Guzman C. A., Pesce A., Schito G. C. 1993; Inhibition of Pseudomonas aeruginosa virulence factors by subinhibitory concentrations of azithromycin and other macrolide antibiotics. J Antimicrob Chemother 31:681–688
    [Google Scholar]
  85. Morfeldt E., Taylor D., von Gabain A., Arvidson S. 1995; Activation of α-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14:4569–4577
    [Google Scholar]
  86. Musser J. M., Schlievert P. M., Chow A. W., Ewan P., Kreiswirth B. N., Rosdahl V. T., Naidu A. S., Witte W., Selander R. K. 1990; A single clone of Staphylococcus aureus causes the majority of cases of toxic shock syndrome. Proc Natl Acad Sci U S A 87:225–229
    [Google Scholar]
  87. Ng W. L., Bassler B. L. 2009; Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222
    [Google Scholar]
  88. Novick R. P., Geisinger E. 2008; Quorum sensing in staphylococci. Annu Rev Genet 42:541–564
    [Google Scholar]
  89. Novick R. P., Projan S. J., Kornblum J., Ross H. F., Ji G., Kreiswirth B., Vandenesch F., Moghazeh S. 1995; The agr P2 operon: an autocatalytic sensory transduction system in Staphylococcus aureus. Mol Gen Genet 248:446–458
    [Google Scholar]
  90. Oglesby A. G., Farrow J. M. III, Lee J. H., Tomaras A. P., Greenberg E. P., Pesci E. C., Vasil M. L. 2008; The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283:15558–15567
    [Google Scholar]
  91. Otto M., Sussmuth R., Jung G., Gotz F. 1998; Structure of the pheromone peptide of the Staphylococcus epidermidis agr system. FEBS Lett 424:89–94
    [Google Scholar]
  92. Parsek M. R., Tolker-Nielsen T. 2008; Pattern formation in Pseudomonas aeruginosa biofilms. Curr Opin Microbiol 11:560–566
    [Google Scholar]
  93. Patriquin G. M., Banin E., Gilmour C., Tuchman R., Greenberg E. P., Poole K. 2008; Influence of quorum sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 190:662–671
    [Google Scholar]
  94. Persson T., Hansen T. H., Rasmussen T. B., Skinderso M. E., Givskov M., Nielsen J. 2005; Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 3:253–262
    [Google Scholar]
  95. Pesci E. C., Milbank J. B., Pearson J. P., McKnight S., Kende A. S., Greenberg E. P., Iglewski B. H. 1999; Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 96:11229–11234
    [Google Scholar]
  96. Pottathil M., Lazazzera B. A. 2003; The extracellular Phr peptide–Rap phosphatase signaling circuit of Bacillus subtilis. Front Biosci 8:d32–d45
    [Google Scholar]
  97. Rahme L. G., Tan M. W., Le L., Wong S. M., Tompkins R. G., Calderwood S. B., Ausubel F. M. 1997; Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc Natl Acad Sci U S A 94:13245–13250
    [Google Scholar]
  98. Rahme L. G., Ausubel F. M., Cao H., Drenkard E., Goumnerov B. C., Lau G. W., Mahajan-Miklos S., Plotnikova J., Tan M. W. 2000; Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97:8815–8821
    [Google Scholar]
  99. Rasko D. A., Moreira C. G., de Li R., Reading N. C., Ritchie J. M., Waldor M. K., Williams N., Taussig R., Wei S. other authors 2008; Targeting QseC signaling and virulence for antibiotic development. Science 321:1078–1080
    [Google Scholar]
  100. Rasmussen T. B., Bjarnsholt T., Skindersoe M. E., Hentzer M., Kristoffersen P., Kote M., Nielsen J., Eberl L., Givskov M. 2005a; Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814
    [Google Scholar]
  101. Rasmussen T. B., Skindersoe M. E., Bjarnsholt T., Phipps R. K., Christensen K. B., Jensen P. O., Andersen J. B., Koch B., Larsen T. O. other authors 2005b; Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325–1340
    [Google Scholar]
  102. Reading N. C., Rasko D. A., Torres A. G., Sperandio V. 2009; The two-component system QseEF and the membrane protein QseG link adrenergic and stress sensing to bacterial pathogenesis. Proc Natl Acad Sci U S A 106:5889–5894
    [Google Scholar]
  103. Rezzonico F., Duffy B. 2008; Lack of genomic evidence of AI-2 receptors suggests a non-quorum sensing role for luxS in most bacteria. BMC Microbiol 8:154
    [Google Scholar]
  104. Roux A., Payne S. M., Gilmore M. S. 2009; Microbial telesensing: probing the environment for friends, foes, and food. Cell Host Microbe 6:115–124
    [Google Scholar]
  105. Saenz H. L., Augsburger V., Vuong C., Jack R. W., Gotz F., Otto M. 2000; Inducible expression and cellular location of AgrB, a protein involved in the maturation of the staphylococcal quorum-sensing pheromone. Arch Microbiol 174:452–455
    [Google Scholar]
  106. Saiman L., Marshall B. C., Mayer-Hamblett N., Burns J. L., Quittner A. L., Cibene D. A., Coquillette S., Fieberg A. Y., Accurso F. J. other authors 2003; Azithromycin in patients with cystic fibrosis chronically infected with Pseudomonas aeruginosa: a randomized controlled trial. JAMA 290:1749–1756
    [Google Scholar]
  107. Sandoz K. M., Mitzimberg S. M., Schuster M. 2007; Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 104:15876–15881
    [Google Scholar]
  108. Schaber J. A., Carty N. L., McDonald N. A., Graham E. D., Cheluvappa R., Griswold J. A., Hamood A. N. 2004; Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa. J Med Microbiol 53:841–853
    [Google Scholar]
  109. Schauder S., Shokat K., Surette M. G., Bassler B. L. 2001; The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41:463–476
    [Google Scholar]
  110. Schuster M., Greenberg E. P. 2006; A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296:73–81
    [Google Scholar]
  111. Schuster M., Lostroh C. P., Ogi T., Greenberg E. P. 2003; Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185:2066–2079
    [Google Scholar]
  112. Singh P. K., Schaefer A. L., Parsek M. R., Moninger T. O., Welsh M. J., Greenberg E. P. 2000; Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764
    [Google Scholar]
  113. Skindersoe M. E., Zeuthen L. H., Brix S., Fink L. N., Lazenby J., Whittall C., Williams P., Diggle S. P., Froekiaer H. other authors 2009; Pseudomonas aeruginosa quorum-sensing signal molecules interfere with dendritic cell-induced T-cell proliferation. FEMS Immunol Med Microbiol 55:335–345
    [Google Scholar]
  114. Smith R. S., Iglewski B. H. 2003; P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56–60
    [Google Scholar]
  115. Smith R. S., Harris S. G., Phipps R., Iglewski B. 2002; The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo. J Bacteriol 184:1132–1139
    [Google Scholar]
  116. Smith D., Wang J. H., Swatton J. E., Davenport P., Price B., Mikkelsen H., Stickland H., Nishikawa K., Gardiol N. other authors 2006; Variations on a theme: diverse N-acyl homoserine lactone-mediated quorum sensing mechanisms in Gram-negative bacteria. Sci Prog 89:167–211
    [Google Scholar]
  117. Sofer D., Gilboa-Garber N., Belz A., Garber N. C. 1999; ‘Subinhibitory’ erythromycin represses production of Pseudomonas aeruginosa lectins, autoinducer and virulence factors. Chemotherapy 45:335–341
    [Google Scholar]
  118. Sperandio V., Mellies J. L., Nguyen W., Shin S., Kaper J. B. 1999; Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96:15196–15201
    [Google Scholar]
  119. Sperandio V., Torres A. G., Giron J. A., Kaper J. B. 2001; Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157 : H7. J Bacteriol 183:5187–5197
    [Google Scholar]
  120. Sperandio V., Li C. C., Kaper J. B. 2002a; Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 70:3085–3093
    [Google Scholar]
  121. Sperandio V., Torres A. G., Kaper J. B. 2002b; Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43:809–821
    [Google Scholar]
  122. 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 U S A 100:8951–8956
    [Google Scholar]
  123. Surette M. G., Bassler B. L. 1998; Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci U S A 95:7046–7050
    [Google Scholar]
  124. Surette M. G., Miller M. B., Bassler B. L. 1999; Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A 96:1639–1644
    [Google Scholar]
  125. Swift S., Downie J. A., Whitehead N. A., Barnard A. M., Salmond G. P., Williams P. 2001; Quorum sensing as a population-density-dependent determinant of bacterial physiology. Adv Microb Physiol 45:199–270
    [Google Scholar]
  126. Taga M. E., Semmelhack J. L., Bassler B. L. 2001; The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium. Mol Microbiol 42:777–793
    [Google Scholar]
  127. Tateda K., Comte R., Pechere J. C., Kohler T., Yamaguchi K., Van Delden C. 2001; Azithromycin inhibits quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 45:1930–1933
    [Google Scholar]
  128. Tateda K., Ishii Y., Horikawa M., Matsumoto T., Miyairi S., Pechere J. C., Standiford T. J., Ishiguro M., Yamaguchi K. 2003; The Pseudomonas aeruginosa autoinducer N-3-oxododecanoyl homoserine lactone accelerates apoptosis in macrophages and neutrophils. Infect Immun 71:5785–5793
    [Google Scholar]
  129. Telford G., Wheeler D., Williams P., Tomkins P. T., Appleby P., Sewell H., Stewart G. S., Bycroft B. W., Pritchard D. I. 1998; The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun 66:36–42
    [Google Scholar]
  130. Vandeputte O. M., Kiendrebeogo M., Rajaonson S., Diallo B., Mol A., El Jaziri M., Baucher M. 2010; Identification of catechin as one of the flavonoids from Combretum albiflorum bark extract that reduces the production of quorum-sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 76:243–253
    [Google Scholar]
  131. Vuong C., Saenz H. L., Gotz F., Otto M. 2000; Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J Infect Dis 182:1688–1693
    [Google Scholar]
  132. Wagner V. E., Bushnell D., Passador L., Brooks A. I., Iglewski B. H. 2003; Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185:2080–2095
    [Google Scholar]
  133. Walters M., Sperandio V. 2006; Quorum sensing in Escherichia coli and Salmonella. Int J Med Microbiol 296:125–131
    [Google Scholar]
  134. Wescombe P. A., Tagg J. R. 2003; Purification and characterization of streptin, a type A1 lantibiotic produced by Streptococcus pyogenes. Appl Environ Microbiol 69:2737–2747
    [Google Scholar]
  135. West S. A., Griffin A. S., Gardner A., Diggle S. P. 2006; Social evolution theory for microorganisms. Nat Rev Microbiol 4:597–607
    [Google Scholar]
  136. Whitehead N. A., Barnard A. M., Slater H., Simpson N. J., Salmond G. P. 2001; Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404
    [Google Scholar]
  137. Winzer K., Hardie K. R., Williams P. 2002; Bacterial cell-to-cell communication: sorry, can't talk now – gone to lunch!. Curr Opin Microbiol 5:216–222
    [Google Scholar]
  138. Wright J. S. III, Traber K. E., Corrigan R., Benson S. A., Musser J. M., Novick R. P. 2005; The agr radiation: an early event in the evolution of staphylococci. J Bacteriol 187:5585–5594
    [Google Scholar]
  139. Xiao G., Déziel E., He J., Lépine F., Lesic B., Castonguay M. H., Milot S., Tampakaki A. P., Stachel S. E., Rahme L. G. 2006; MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689–1699
    [Google Scholar]
  140. Yao Y., Vuong C., Kocianova S., Villaruz A. E., Lai Y., Sturdevant D. E., Otto M. 2006; Characterization of the Staphylococcus epidermidis accessory-gene regulator response: quorum-sensing regulation of resistance to human innate host defense. J Infect Dis 193:841–848
    [Google Scholar]
  141. Yarwood J. M., Bartels D. J., Volper E. M., Greenberg E. P. 2004; Quorum sensing in Staphylococcus aureus biofilms. J Bacteriol 186:1838–1850
    [Google Scholar]
  142. Yoon S. S., Hennigan R. F., Hilliard G. M., Ochsner U. A., Parvatiyar K., Kamani M. C., Allen H. L., DeKievit T. R., Gardner P. R. other authors 2002; Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3:593–603
    [Google Scholar]
  143. Zhang L., Lin J., Ji G. 2004; Membrane anchoring of the AgrD N-terminal amphipathic region is required for its processing to produce a quorum-sensing pheromone in Staphylococcus aureus. J Biol Chem 279:19448–19456
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.038794-0
Loading
/content/journal/micro/10.1099/mic.0.038794-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error