Quorum Sensing in Pseudomonas aeruginosa: Mechanism and Regulation of Virulence

  • Sajal Sarabhai
  • Amanjot Kaur
  • Neena Capalash
  • Prince Sharma
Chapter
First Online:

Abstract

P. aeruginosa is the causative agent of nosocomial infections, especially in immunocompromised and burn patients and causes chronic infections in cystic fibrosis patients. The intrinsic resistance of P. aeruginosa against different antibiotic groups led to the emergence of multiple drug resistance thereby making its eradication difficult. An array of cell associated and extracellular virulence factors have made this organism capable to habitat any type of tissue. Quorum sensing is the global regulatory network in P. aeruginosa capable of regulating the expression of virulence and hence its pathogenicity. There are a total of four QS systems in P. aeruginosa, viz., LasIR, RhlIR, PQS and IQS, interconnected to each other through various pathways, hence regulating the expression of various target virulence genes. The interference in QS system attenuates P. aeruginosa, hence making its eradication more easy. This strategy has been emerged as an alternative method of targeting P. aeruginosa infection and the basis of future medicines.

Keywords

Virulence Factor Cystic Fibrosis Patient Quorum Sense Alkaline Protease Quorum Sense System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
This is a preview of subscription content, log in to check access.

References

  1. Adonizio A, Kong KF, Mathee K (2008) Inhibition of quorum sensing controlled virulence factor production in Pseudomonas aeruginosa by south florida plant extracts. Antimicrob Agents Chemother 52:198–203PubMedPubMedCentralCrossRefGoogle Scholar
  2. Albus AM, Pesci EC, Runyen-Janecky LJ et al (1997) Vfr controls quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3928–3935PubMedPubMedCentralGoogle Scholar
  3. Aloush V, Navon-Venezia S, Seigman-Igra Y et al (2006) Multidrug-resistant Pseudomonas aeruginosa: risk factors and clinical impact. Antimicrob Agents Chemother 50(1):43–48PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bergey (2001) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New YorkGoogle Scholar
  5. 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 70:5493–5502PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bjarnsholt T, Jensen PO, Rasmussen TB et al (2005) Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151:3873–3880PubMedCrossRefGoogle Scholar
  7. Brackman G, Cos P, Maes L et al (2011) Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother 55(6):2655–2661PubMedPubMedCentralCrossRefGoogle Scholar
  8. Branny P, Pearson JP, Pesci EC et al (2001) Inhibition of quorum sensing by a Pseudomonas aeruginosa dksA homologue. J Bacteriol 183:1531–1539PubMedPubMedCentralCrossRefGoogle Scholar
  9. Brencic A, McFarland KA, McManus HR et al (2009) The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 73:434–445PubMedPubMedCentralCrossRefGoogle Scholar
  10. Caballero AR, Moreau JM, Engel LS et al (2001) Pseudomonas aeruginosa protease IV enzyme assays and comparison to other pseudomonas protease. Anal Biochem 290(2):330–337PubMedCrossRefGoogle Scholar
  11. Caiazza NC, Robert MQ, Shanks RM et al (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187(21):7351PubMedPubMedCentralCrossRefGoogle Scholar
  12. Calfee MW, Coleman JP, Pesci EC (2001) Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 98:11633–11637PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cao H, Krishnan G, Goumnerov B et al (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 98:14613–14618PubMedPubMedCentralCrossRefGoogle Scholar
  14. Choo JH, Rukayadi Y, Hwang JK (2006) Inhibition of bacterial quorum sensing by vanilla extract. Lett Appl Microbiol 42:637–641PubMedGoogle Scholar
  15. Chugani SA, Whiteley M, Lee KM et al (2001) QscR, a modulator of quorum-sensing signal synthesis and virulence in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 98:2752–2757PubMedPubMedCentralCrossRefGoogle Scholar
  16. Cox CD (1982) Effect of pyochelin on the virulence of Pseudomonas aeruginosa. Infect Immun 36:17–23PubMedPubMedCentralGoogle Scholar
  17. Cruickshank CND, Lowbury EJL (1953) The effect of pyocyanin on human skin cells and leucocytes. Br J Exp Pathol 34(6):583–587PubMedPubMedCentralGoogle Scholar
  18. Davey ME, Caiazza NC, O’Toole GA (2003) Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J Bacteriol 185:1027–1036PubMedPubMedCentralCrossRefGoogle Scholar
  19. Davies DG, Parsek MR, Pearson JP et al (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280(5361):295–298PubMedCrossRefGoogle Scholar
  20. de Kievit T, Seed PC, Nezezon J et al (1999) RsaL, a novel repressor of virulence gene expression in Pseudomonas aeruginosa. J Bacteriol 181:2175–2184PubMedPubMedCentralGoogle Scholar
  21. Dekimpe V, Deziel E (2009) Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155:712–723PubMedCrossRefGoogle Scholar
  22. Denning GM, Iyer SS, Reszka KJ et al (2003) Phenazine-1-carboxylic acid, a secondary metabolite of Pseudomonas aeruginosa, alters expression of immunomodulatory proteins by human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 285:584–592CrossRefGoogle Scholar
  23. Denning GM, Railsback MA, Rasmussen GT et al (1998) Pseudomonas pyocyanin increases interleukin-8 expression by human airway epithelial cells. Infect Immun 66:5777–5784PubMedPubMedCentralGoogle Scholar
  24. Deziel E, Lepine F, Milot S et al (2003) rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa 3-(3-hydroxyalkanoyloxy)alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149:2005–2013PubMedCrossRefGoogle Scholar
  25. Deziel E, Lepine F, Milot S et al (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 101:1339–1344PubMedPubMedCentralCrossRefGoogle Scholar
  26. Deziel E, Gopalan S, Tampakaki A et al (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(4):998–1014PubMedCrossRefGoogle Scholar
  27. Diggle SP, Winzer K, Lazdunski A et al (2002) Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J Bacteriol 184:2576–2586PubMedPubMedCentralCrossRefGoogle Scholar
  28. Diggle SP, Winzer K, Chhabra SR et al (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 50:29–43PubMedCrossRefGoogle Scholar
  29. Dong YH, Zhang XF, Soo HM et al (2005) The two-component response regulator PprB modulates quorum-sensing signal production and global gene expression in Pseudomonas aeruginosa. Mol Microbiol 56:1287–1301PubMedCrossRefGoogle Scholar
  30. Edwards JR, Richard MJ, Culver DH et al (2007) Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 21(8):510–515Google Scholar
  31. Espinosa-Urgel M (2003) Resident parking only: rhamnolipids maintain fluid channels in biofilms. J Bacteriol 185:699–700PubMedPubMedCentralCrossRefGoogle Scholar
  32. Flanders SA, Collard HR, Saint S (2006) Nosocomial pneumonia: state of the science. Am J Infect Control 34:84–93PubMedCrossRefGoogle Scholar
  33. Foca MD (2002) Pseudomonas aeruginosa infections in the neonatal intensive care unit. Semin Perinatol 26:332–339PubMedCrossRefGoogle Scholar
  34. Fraley CD, Rashid MH, Lee SSK et al (2007) A polyphosphate kinase 1 (pp k1) mutant of Pseudomonas aeruginosa exhibits multiple ultrastructural and functional defects. Proc Nat Acad Sci USA 104:3526–3530PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275PubMedPubMedCentralGoogle Scholar
  36. Gallagher LA, McKnight SL, Kuznetsova MS et al (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184:6472–6480PubMedPubMedCentralCrossRefGoogle Scholar
  37. Geske GD, O’Neill JC, Miller DM et al (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 129:13613–13625PubMedPubMedCentralCrossRefGoogle Scholar
  38. Gibson RL, Burns JL, Ramsey BW (2003) Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 168(8):918–951PubMedCrossRefGoogle Scholar
  39. Hassett DJ, Ma JF, Elkins JG et al (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34:1082–1093PubMedCrossRefGoogle Scholar
  40. Hastie AT, Hingley ST, Higgins ML et al (1986) Rhamnolipid from Pseudomonas aeruginosa inactivates mammalian tracheal ciliary axonemes. Cell Motil Cytoskeleton 6:502–509PubMedCrossRefGoogle Scholar
  41. Heeb S, Blumer C, Haas D (2002) Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol 184:1046–1056PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hengge-aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66(3):373–395PubMedPubMedCentralCrossRefGoogle Scholar
  43. Hentzer M, Teitzel GM, Balzer GJ et al (2001) Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol 183:5395–5401PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hentzer M, Wu H, Andersen JB et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitor. EMBO J 22:3803–3815PubMedPubMedCentralCrossRefGoogle Scholar
  45. Heurlier K, Denervaud V, Pessi G et al (2003) Negative control of quorum sensing by RpoN (sigma54) in Pseudomonas aeruginosa PAO1. J Bacteriol 185:2227–2235PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hoge R, Pelzer A, Rosenan F et al (2010) Weapons of a pathogen: proteases and their role in virulence of Pseudomonas aeruginosa. In: Mendez-Vilas A (ed) Current research technology and education topics in applied microbiology and microbial biotechnology, vol 2. Formatex Research Center, pp 383–395Google Scholar
  47. Hommais F, Krin E, Laurent-Winter C et al (2001) Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol 40(1):20–36PubMedCrossRefGoogle Scholar
  48. Howe TR, Iglewski BH (1984) Isolation and characterization of alkaline protease-deficient mutants of Pseudomonas aeruginosa in vitro and in a mouse eye model. Infect Immun 43:1058–1063PubMedPubMedCentralGoogle Scholar
  49. Huber B, Eberl L, Feucht W et al (2003) Influence of polyphenols on bacterial biofilm formation and quorum sensing. Z Naturforsch 58:879–884Google Scholar
  50. Jensen PO, Bjarnsholt T, Phipps R et al (2007) Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiol 153:1329–1338CrossRefGoogle Scholar
  51. Joseph NM, Devi S, Shashikala P et al (2013) Changing trend in the antibiotic resistance pattern of Pseudomonas aeruginosa isolated from wound swabs of out-patients and in-patients of a tertiary care hospital. J Clin Diag Res 7(10):2170–2172Google Scholar
  52. Jude F, Kohler T, Branny P et al (2003) Posttranscriptional control of quorum-sensing-dependent virulence genes by DksA in Pseudomonas aeruginosa. J Bacteriol 185:3558–3566PubMedPubMedCentralCrossRefGoogle Scholar
  53. Juhas M, Wiehlmann L, Huber B et al (2004) Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150:831–841PubMedCrossRefGoogle Scholar
  54. Juhas M, Wiehlmann L, Salunkhe P et al (2005) GeneChip expression analysis of the VqsR regulon of Pseudomonas aeruginosa TB. FEMS Microbiol Lett 242:287–295PubMedCrossRefGoogle Scholar
  55. Kalia VC (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31(2):224–245PubMedCrossRefGoogle Scholar
  56. Kiratisin P, Tucker KD, Passador L (2002) LasR, a transcriptional activator of Pseudomonas aeruginosa virulence genes, functions as a multimer. J Bacteriol 184:4912–4919PubMedPubMedCentralCrossRefGoogle Scholar
  57. Köhler T, Ouertatani-Sakouhi H, Cosson P et al (2014) QsrO a novel regulator of quorum-sensing and virulence in Pseudomonas aeruginosa. PLoS One 9(2), e87814. doi: 10.1371/journal.pone.0087814 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kornberg A, Rao NN, Ault-Riche D (1999) Inorganic polyphosphate: A molecule of many functions. Ann Rev Biochem 68:89–125Google Scholar
  59. Krcmery V, Koprnova J, Gogova M et al (2006) Pseudomonas aeruginosa bacteraemia in cancer patients. J Infect 52:461–463PubMedCrossRefGoogle Scholar
  60. Lang S, Wullbrandt D (1999) Rhamnose lipids-biosynthesis, microbial production and application potential. Appl Microbiol Biotechnol 51:22–32PubMedCrossRefGoogle Scholar
  61. Latifi A, Foglino M, Tanaka K et al (1996) 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 21:1137–1146PubMedCrossRefGoogle Scholar
  62. Ledgham F, Soscia C, Chakrabarty A et al (2003a) Global regulation in Pseudomonas aeruginosa: the regulatory protein AlgR2 (AlgQ) acts as a modulator of quorum sensing. Res Microbiol 154:207–213PubMedCrossRefGoogle Scholar
  63. Ledgham F, Ventre I, Soscia C et al (2003b) Interactions of the quorum sensing regulator QscR: interaction with itself and the other regulators of Pseudomonas aeruginosa LasR and RhlR. Mol Microbiol 48:199–210PubMedCrossRefGoogle Scholar
  64. Lee J, Wu J, Deng Y et al (2013) A cell-cell communication signal integrates quorum sensing and stress response. Nat Chem Biol 9:339–343PubMedCrossRefGoogle Scholar
  65. Liang H, Deng X, Ji Q et al (2012) The Pseudomonas aeruginosa global regulator VqsR directly inhibits QscR to control Quorum-Sensing and virulence gene expression. J Bacteriol 194:3098–3108PubMedPubMedCentralCrossRefGoogle Scholar
  66. Maier RM, Soberón-Chávez G (2000) Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl Microbiol Biotechnol 54:625–633PubMedCrossRefGoogle Scholar
  67. Marshall KC (1992) Biofilms: an overview of bacterial adhesion, activity and control at surface. ASM News 58:202–207Google Scholar
  68. McClure CD, Schiller NL (1992) Effects of Pseudomonas aeruginosa rhamnolipids on human monocyte-derived macrophages. J Leukocyte Biol 51:97–102PubMedGoogle Scholar
  69. McKnight SL, Iglewski BH, Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 182:2702–2708PubMedPubMedCentralCrossRefGoogle Scholar
  70. Medina G, Juarez K, Diaz R et al (2003) Transcriptional regulation of Pseudomonas aeruginosa rhlR, encoding a quorum-sensing regulatory protein. Microbiology 149:3073–3081PubMedCrossRefGoogle Scholar
  71. Musthafa KS, Ravi AV, Annapoorani A et al (2010) Evaluation of anti-quorum-sensing activity of edible plants and fruits through inhibition of the N-acyl-homoserine lactone system in Chromobacterium violaceum and Pseudomonas aeruginosa. Chemotherapy 56:333–339PubMedCrossRefGoogle Scholar
  72. Nicas TI, Frank DW, Stenzel P et al (1985) Role of exoenzyme S in chronic Pseudomonas aeruginosa lung infections. Eur J Clin Microbiol 4:175–179PubMedCrossRefGoogle Scholar
  73. Niu C, Afre S, Gilbert ES (2006) Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett Appl Microbiol 43(5):489–494PubMedCrossRefGoogle Scholar
  74. Norizan SNM, Yin WF, Chan KG (2013) Caffeine as a potential quorum sensing inhibitor. Sensor 13(4):5117–5129PubMedPubMedCentralCrossRefGoogle Scholar
  75. O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304PubMedCrossRefGoogle Scholar
  76. Ostendorf U, Ewig S, Torres A (2006) Nosocomial pneumonia. Curr Opin Infect Dis 19(4):327–338PubMedCrossRefGoogle Scholar
  77. Overhage J, Bains M, Brazas MD et al (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190(8):2671–2679PubMedPubMedCentralCrossRefGoogle Scholar
  78. Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215–1226PubMedCrossRefGoogle Scholar
  79. Pedersen SS, Hoiby N, Espersen F et al (1992) Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis. Thorax 47:6–13PubMedPubMedCentralCrossRefGoogle Scholar
  80. Persson T, Hansen TH, Rasmussen TB et al (2005) Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org Biomol Chem 3:253–262PubMedCrossRefGoogle Scholar
  81. Pesci E, Pearson J, Seed P et al (1997) Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179:3127–3132PubMedPubMedCentralGoogle Scholar
  82. Pesci EC, Milbank JB, Pearson JP et al (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:11229–11234PubMedPubMedCentralCrossRefGoogle Scholar
  83. Pessi G, Williams F, Hindle Z et al (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and Nacylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183:6676–6683PubMedPubMedCentralCrossRefGoogle Scholar
  84. Preston MJ, Seed PC, Toder DS et al (1997) Contribution of proteases and LasR to the virulence of Pseudomonas aeruginosa during corneal infections. Infect Immun 65:3086–3090PubMedPubMedCentralGoogle Scholar
  85. Rampioni G, Schuster M, Greenberg EP et al (2007) RsaL provides quorum sensing homeostasis and functions as a global regulator of gene expression in Pseudomonas aeruginosa. Mol Microbiol 66:1557–1565PubMedCrossRefGoogle Scholar
  86. Rasmussen TB, Bjarnsholt T, Skindersoe ME et al (2005) Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187:1799–1814PubMedPubMedCentralCrossRefGoogle Scholar
  87. Regules JA, Glasser JS, Wolf SE et al (2008) Endocarditis in burn patients: clinical and diagnostic considerations. Burns 34(5):610–616PubMedCrossRefGoogle Scholar
  88. Reimmann C, Beyeler M, Latifi A et al (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 24:309–319PubMedCrossRefGoogle Scholar
  89. Sarabhai S, Sharma P, Capalash N (2013) Ellagic acid derivatives from Terminalia chebula Retz. downregulate the expression of Quorum Sensing genes to attenuate Pseudomonas aeruginosa PAO1 virulence. PLoS One 8(1), e53441PubMedPubMedCentralCrossRefGoogle Scholar
  90. Schooling SR, Charaf UK, Allison DG et al (2004) A role for rhamnolipid in biofilm dispersion. Biofilms 1:91–99CrossRefGoogle Scholar
  91. Schuster M, Hawkins AC, Harwood CS et al (2004) The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol Microbiol 51:973–985PubMedCrossRefGoogle Scholar
  92. Seed PC, Passador L, Iglewski BH (1995) Activation of the Pseudomonas aeruginosa lasI gene by LasR and the Pseudomonas autoinducer PAI: an autoinduction regulatory hierarchy. J Bacteriol 177:654–659PubMedPubMedCentralGoogle Scholar
  93. Smith KM, Bu Y, Suga H (2003) Library screening for synthetic agonists and antagonists of a Pseudomonas aeruginsa autoinducer. Chem Biol 10:563–571PubMedCrossRefGoogle Scholar
  94. Smith RS, Iglewski BH (2003) Pseudomonas aeruginosa quorum sensing as a potential antimicrobial target. J Clin Invest 112(10):1460–1465PubMedPubMedCentralCrossRefGoogle Scholar
  95. Sorenson RU, Klinger JD, Cash HA et al (1983) In vitro inhibition of lymphocyte proliferation by Pseudomonas aeruginosa phenazine pigments. Infect Immun 41:321–330Google Scholar
  96. Tang H, Kays M, Prince A (1995) Role of Pseudomonas aeruginosa pili in acute pulmonary infection. Infect Immun 63:1278–1285PubMedPubMedCentralGoogle Scholar
  97. Tang HB, DiMango E, Bryan R et al (1996) Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect Immun 64:37–43PubMedPubMedCentralGoogle Scholar
  98. Thompson LS, Webb JS, Rice SA et al (2003) The alternative sigma factor RpoN regulates the quorum sensing gene rhlI in Pseudomonas aeruginosa. FEMS Microbiol Lett 220:187–195PubMedCrossRefGoogle Scholar
  99. Tremblay J, Deziel E (2010) Gene expression in Pseudomonas aeruginosa swarming motility. BMC Genomics 11:587–598PubMedPubMedCentralCrossRefGoogle Scholar
  100. Tremblay J, Richardson AP, Lepine F et al (2007) Self-produced extracellular stimuli modulate the Pseudomonas aeruginosa swarming motility behavior. Environ Microbiol 9(10):2622–2630PubMedCrossRefGoogle Scholar
  101. Vallet I, Diggle SP, Stacey RE et al (2004) Biofilm formation in Pseudomonas aeruginosa: fimbrial cup gene clusters are controlled by the transcriptional regulator MvaT. J Bacteriol 186:2880–2890PubMedPubMedCentralCrossRefGoogle Scholar
  102. Vandeputte OM, Kiendrebeogo M, Rajaonson S et al (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 76:243–253PubMedPubMedCentralCrossRefGoogle Scholar
  103. Vasil ML, Graham LM, Ostroff RM et al (1991) Phospholipase C: molecular biology and contribution to the pathogenesis of Pseudomonas aeruginosa. Antibiot Chemother 44:34–47PubMedCrossRefGoogle Scholar
  104. Vattem DA, Mihalik K, Crixell SH et al (2007) Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78:302–310PubMedCrossRefGoogle Scholar
  105. Ventre I, Goodman AL, Vallet-Gely I et al (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 103:171–176PubMedPubMedCentralCrossRefGoogle Scholar
  106. Ventre I, Ledgham F, Prima V et al (2003) Dimerization of the quorum sensing regulator RhlR: development of a method using EGFP fluorescence anisotropy. Mol Microbiol 48:187–198PubMedCrossRefGoogle Scholar
  107. Wang Q, Frye JG, McClelland M et al (2004) Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity. Mol Microbiol 52:169–187PubMedCrossRefGoogle Scholar
  108. Wang Y, Ha U, Zeng L et al (2003) Regulation of membrane permeability by a two-component regulatory system in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47:95–101PubMedPubMedCentralCrossRefGoogle Scholar
  109. West SE, Sample AK, Runyen-Janecky LJ (1994) The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. J Bacteriol 176(24):7532–7542PubMedPubMedCentralGoogle Scholar
  110. Westblade LF, Ilag LL, Powell AK et al (2004) Studies of the Escherichia coli Rsd-sigma70 complex. J Mol Biol 335:685–692PubMedCrossRefGoogle Scholar
  111. Whiteley M, Lee KM, Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:13904–13909PubMedPubMedCentralCrossRefGoogle Scholar
  112. Whiteley M, Parsek MR, Greenberg EP (2000) Regulation of quorum sensing by RpoS in Pseudomonas aeruginosa. J Bacteriol 182:4356–4360PubMedPubMedCentralCrossRefGoogle Scholar
  113. Wilson R, Pitt T, Taylor G et al (1987) Pyocyanin and 1-hydroxy-phenazine produced by Pseudomonas aeruginosa inhibit the beating of human respiratory cilia in vitro. J Clin Invest 79:221–229PubMedPubMedCentralCrossRefGoogle Scholar
  114. Woods DE, Cryz SJ, Friedman RL et al (1982) Contribution of toxin A and elastase to virulence of Pseudomonas aeruginosa in chronic lung infections of rats. Infect Immun 36:1223–1228PubMedPubMedCentralGoogle Scholar
  115. Xiao G, Déziel E, He J et al (2006) MvfR, a key Pseudomonas aeruginosa pathogenicity LTTR-class regulatory protein, has dual ligands. Mol Microbiol 62:1689–1699PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Sajal Sarabhai
    • 1
  • Amanjot Kaur
    • 1
  • Neena Capalash
    • 2
  • Prince Sharma
    • 1
  1. 1.Department of MicrobiologyPunjab UniversityChandigarhIndia
  2. 2.Department of BiotechnologyPunjab UniversityChandigarhIndia

Personalised recommendations