Biotechnology Letters

, Volume 30, Issue 5, pp 777–790 | Cite as

Towards understanding Pseudomonas aeruginosa burn wound infections by profiling gene expression

  • Piotr Bielecki
  • Justyna Glik
  • Marek Kawecki
  • Vítor A. P. Martins dos Santos
Review

Abstract

Pseudomonas aeruginosa is a key opportunistic pathogen causing severe acute and chronic nosocomial infections in immunocompromised or catheterized patients. It is prevalent in burn wound infections and it is generally multi-drug resistant. Understanding the genetic programs underlying infection is essential to develop highly needed new strategies for prevention and therapy. This work reviews expression profiling efforts conducted worldwide towards gaining insights into pathogenesis by P. aeruginosa, in particular in burn wounds. Work on various infection models, including the burned mouse model, has identified several direct virulence factors and elucidated their mode of action. In vivo gene expression experiments using In vivo Expression Technology (IVET) ascertained distinct regulatory circuits and traits that have helped explain P. aeruginosa´s success as a general pathogen. The sequencing of the whole genome from a number of P. aeruginosa strains and the construction of genome-wide microarrays have paved the road to the several insightful studies on the (interacting) traits underlying infection. A series of in vitro and initial in vivo gene expression studies revealed specific traits pivotal for infection, such as quorum sensing systems, iron acquisition and oxidative stress responses, and toxin production among others. The data sets obtained from global transcriptional profiling provide insights that will be essential for the development of new targets and options for prevention and intervention.

Keywords

Burn wound infection Global transcription profiling Microarrays Pseudomonas aeruginosa 

Notes

Acknowledgments

We gratefully acknowledge Andrew Oxley, Melissa Wos and Susanne Häuβler for valuable discussions over the manuscript.

References

  1. Aendekerk S, Diggle SP, Song Z, Hoiby N, Cornelis P, Williams P, Camara M (2005) The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151(4):1113–1125PubMedCrossRefGoogle Scholar
  2. Albus AM, Pesci EC, Runyen-Janecky LJ, West SE, Iglewski BH (1997) Vfr controls quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179(12):3928–3925PubMedGoogle Scholar
  3. Altoparlak U, Erol S, Akcay MN, Celebi F, Kadanali A (2004) The time-related changes of antimicrobial resistance patterns and predominant bacterial profiles of burn wounds and body flora of burned patients. Burns 30(7):660–664PubMedCrossRefGoogle Scholar
  4. Arora SK, Neely AN, Blair B, Lory S, Ramphal R (2005) Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect Immun 73(7):4395–4398PubMedCrossRefGoogle Scholar
  5. Bagge N, Schuster M, Hentzer M, Ciofu O, Givskov M, Greenberg EP, Høiby N (2004) Pseudomonas aeruginosa biofilm exposed to imipenem exhibit changes in global gene expression and ß-lactamase and alginate production. Antimicrob Agents Chemother 48(4):1175–1187PubMedCrossRefGoogle Scholar
  6. Banin E, Vasil ML, Greenberg EP (2005) Iron and P. aeruginosa biofilm formation. Proc Natl Acad Sci USA 102(31):11076–11081PubMedCrossRefGoogle Scholar
  7. Bjarnsholt T, Jensen PØ. Rasmussen TB, Christophersen L, Calum H, Hentzer M, Hougen HP, Rygaard J, Moser C, Eberl L, Høiby N, Givskov M (2005) Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151(12):3873–3880PubMedCrossRefGoogle Scholar
  8. Braun V, Braun M (2002) Iron transport and signalling in Escherichia coli. FEBS Lett 529(1):78–85PubMedCrossRefGoogle Scholar
  9. Bredenbruch F, Geffers R, Nimtz M, Bauer J, Häussler S (2006) The Pseudomonas aeruginosa quinolone signal (PQS) has an iron-chelating activity. Environ Microbiol 8(8):1318–1329PubMedCrossRefGoogle Scholar
  10. Budzikiewicz H (2001) Siderophore-antibiotic conjugates used as trojan horses against Pseudomonas aeruginosa. Curr Top Med Chem 1(1):73–82PubMedCrossRefGoogle Scholar
  11. Chang W, Small DA, Toghrol F, Bentley WE (2005) Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genom 8(6):115CrossRefGoogle Scholar
  12. Chitkara YK, Feierabend TC (1981) Endogenous and exogenous infection with Pseudomonas aeruginosa in a burns unit. Int Surgery 66(1981):237–240Google Scholar
  13. Chugani S, Greenberg EP (2007) The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microb Pathog 42(1):29–35PubMedCrossRefGoogle Scholar
  14. Church D, Elsayed S, Reid O, Winston B, Lindsay R (2006) Burn Wound Infections. Clin Microbiol Rev 19(2): 403–434PubMedCrossRefGoogle Scholar
  15. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280(5361):295–298PubMedCrossRefGoogle Scholar
  16. De Kievit TR, Gillis R, Marx S, Brown C, Iglewski BH (2001) Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67(4):1865–1873PubMedCrossRefGoogle Scholar
  17. Deziel E, Gopalan S, Tampakaki AP, Lepine F, Padfield KE, Saucier M 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
  18. Diggle SP, Winzer K, Chhabra SR, Worrall KE, Camara 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(1):29–43PubMedCrossRefGoogle Scholar
  19. Diggle SP, Cornelis P, Williams P, Camara M (2006) 4-quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 296(23):83–91PubMedCrossRefGoogle Scholar
  20. Diggle SP, Matthijs S, Wright VJ, Fletcher MP, Chhabra SR, Lamont IL, Kong X, Hider RC, Cornelis P, Cámara M, Williams P (2007) The Pseudomonas aeruginosa 4-quinolone signal molecules HHQ and PQS play multifunctional roles in quorum sensing and iron entrapment. Chem Biol 14(1):87–96PubMedCrossRefGoogle Scholar
  21. Dong YH, Zhang XF, Soo HM, Greenberg EP, Zhang LH (2005) The two-component response regulator PprB modulates quorum-sensing signal production and global gene expression in Pseudomonas aeruginosa. Mol Microbiol 56(5):1287–1301PubMedCrossRefGoogle Scholar
  22. Ehrlich GD, Veeh R, Wang X, Costerton JW, Hayes JD, Hu FZ, Daigle BJ, Ehrlich MD, Post JC (2002) Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287(13):1710–1715PubMedCrossRefGoogle Scholar
  23. Ferreras JA, Ryu JS, Di Lello F, Tan DS, Quadri LE (2005) Small-molecule inhibition of siderophore biosynthesis in Mycobacterium tuberculosis and Yersinia pestis. Nat Chem Biol (1):29–32Google Scholar
  24. 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(9):5433–5438PubMedCrossRefGoogle Scholar
  25. Furci LM, Lopes P, Eakanunkul S, Zhong S, MacKerell AD, Wilks A (2007) Inhibition of the bacterial heme oxygenases from Pseudomonas aeruginosa and Neisseria meningitidis: novel antimicrobial targets. J Med Chem 50(16):3804–3813PubMedCrossRefGoogle Scholar
  26. Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184(23):6472–6480PubMedCrossRefGoogle Scholar
  27. Givskov M, de Nys R, Manfield M, Gram L, Maximilien R, Eberl L, Molin S, Steinberg PD, Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178(22):6618–6622PubMedGoogle Scholar
  28. Goodman AL, Lory S (2004) Analysis of regulatory networks in Pseudomonas aeruginosa by genomewide transcriptional profiling. Curr Opin Microbiol 7(1):39–44PubMedCrossRefGoogle Scholar
  29. Ha U, Jin S (1999) Expression of the soxR gene of Pseudomonas aeruginosa is inducible during infection of burn wounds in mice and is required to cause efficient bacteremia. Infect Immun 67(10):5324–5331PubMedGoogle Scholar
  30. Ha UH, Kim J, Badrane H, Jia J, Baker HV, Wu D, Jin S (2004) An in vivo inducible gene of Pseudomonas aeruginosa encodes an anti-ExsA to suppress the type III secretion system. Mol Microbiol 54(2):307–320PubMedCrossRefGoogle Scholar
  31. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microb 2(2):95–108CrossRefGoogle Scholar
  32. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22(15):3803–3815PubMedCrossRefGoogle Scholar
  33. Hentzer M, Eberl L, Givskov M (2005) Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2(1):37–61CrossRefGoogle Scholar
  34. Heydorn A, Ersboll B, Kato J, Hentzer M, Parsek MR, Tolker-Nielsen T, Givskov M, Molin S (2002) Statistical analysis of Pseudomonas aeruginosa biofilm development: impact of mutations in genes involved in twitching motility, cell-to-cell signaling and stationary-phase sigma factor expression. App Environ Microbiol 68(4):2008–2017CrossRefGoogle Scholar
  35. Hoffman LR, Déziel E, D’Argenio DA, Lépine F, Emerson J (2006) Selection for Staphylococcus aureus small-colony variants due to growth in the presence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 103(52):19890–19895PubMedCrossRefGoogle Scholar
  36. Hoffman N, Lee B, Hentzer M, Rasmussen TB, Song Z, Johansen HK, Givskov M, Hoiby N (2007) Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr -/- Mice. Antimicrob Agents Chemother 51(10):3677–3687CrossRefGoogle Scholar
  37. Hsueh PR, Teng LJ, Yang PC, Chen YC, Ho SW, Luh KT (1998) Persistence of a multidrug-resistant Pseudomonas aeruginosa clone in an intensive care burn unit. J Clin Microbiol (36):1347–1351Google Scholar
  38. Juhas M, Wiehlmann L, Salunkhe P, Lauber J, Buer J, Tümmler B (2005) GeneChip expression analysis of the VqsR regulon of Pseudomonas aeruginosa TB. FEMS Microbiol Lett 242(2):287–295PubMedCrossRefGoogle Scholar
  39. Konig B, Vasil ML, Konig W (1997) Role of hemolytic and nonhemolytic phospholipase C from Pseudomonas aeruginosa for inflammatory mediator release from human granulocytes. Int Arch Allergy Immunol 112(2):115–124PubMedCrossRefGoogle Scholar
  40. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 99(10):7072–7077PubMedCrossRefGoogle Scholar
  41. Larocque RC, Harris JB, Dziejman M, Li X, Khan AI, Faruque AS, Faruque SM, Nair GB, Ryan ET, Qadri F, Mekalanos JJ, Calderwood SB (2005) Transcriptional profiling of Vibrio cholerae recovered directly from patient specimens during early and late stages of human infection. Infect Immun 73(8):4488–4493PubMedCrossRefGoogle Scholar
  42. Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL et al (2006) Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7(10):R90PubMedCrossRefGoogle Scholar
  43. Lequette Y, Lee JH, Ledgham F, Lazdunski A, Greenberg EP (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188(9):3365–3370PubMedCrossRefGoogle Scholar
  44. Létoffé S, Redeker V, Wandersman C (1998) Isolation and characterization of an extracellular haem-binding protein from Pseudomonas aeruginosa that shares function and sequence similarities with the Serratia marcescens HasA haemophore. Mol Microbiol 28(6):1223–1234PubMedCrossRefGoogle Scholar
  45. Lyczak BJ, Cannon CL, Pier GB (2002) Lung infections associated with cystic fibrosis. Clin Microb Rev 15(2):194–222CrossRefGoogle Scholar
  46. Mahan MJ, Slauch JM, Mekalanos JJ (1993) Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259(5095):686–688PubMedCrossRefGoogle Scholar
  47. Manefield M, Rasmussen TB, Hentzer M, Andersen JB, Steinberg P, Kjelleberg S, Givskov M (2002) Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. Microbiology 148(4):1119–1127PubMedGoogle Scholar
  48. Mashburn LM, Jett AM, Akins DR, Whiteley M (2005) Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture. J Bacteriol 187(2):554–566PubMedCrossRefGoogle Scholar
  49. McKnight SL, Iglewski BH, Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 182(10):2702–2708PubMedCrossRefGoogle Scholar
  50. Nalca Y, Jänsch L, Bredenbruch F, Geffers R, Buer J, Häussler S (2006) Quorum-sensing antagonistic activities of azithromycin in Pseudomonas aeruginosa PAO1: a global approach. Antimicrob Agents Chemiother 50(5):1680–1688CrossRefGoogle Scholar
  51. Nicas TT, Iglewski BH (1985) The contribution of exoproducts to virulence of Pseudomonas aeruginosa. Can J Microbiol 31(4):387–392PubMedCrossRefGoogle Scholar
  52. 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(5):1277–1287PubMedCrossRefGoogle Scholar
  53. Palma M, Worgall S, Quadri LE (2003) Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch Microbiol 180(5):374–379PubMedCrossRefGoogle Scholar
  54. Palma M, DeLuca D, Worgall S, Quadri LE (2004) Transcriptome analysis of the response of Pseudomonas aeruginosa to hydrogen peroxide. J Bacteriol 186(1):248–252PubMedCrossRefGoogle Scholar
  55. Palma M, Zurita J, Ferreras JA, Worgall S, Larone DH, Shi L, Campagne F, Quadri LE (2005) Pseudomonas aeruginosa SoxR does not conform to the archetypal paradigm for SoxR-dependent regulation of the bacterial oxidative stress adaptive response. Infect Immun 73(5):2958–2966PubMedCrossRefGoogle Scholar
  56. Pavlovskis OR, Wretlind B (1979) Assesment of protease (elastase) as a Pseudomonas aeruginosa virulence factor in experimental mouse burn infection. Infect Immun 24(1):181–187PubMedGoogle Scholar
  57. 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(20):11229–11234PubMedCrossRefGoogle Scholar
  58. Quadri LEN (2007) Strategic paradigm shifts in the antimicrobial drug discovery process of the 21st century. Infect Disord Drug Targets 7(3):230–237PubMedGoogle Scholar
  59. Rainey PB, Preston GM (2000) In vivo expression technology strategies: valuable tools for biotechnology. Curr Opin Biotechnol 11(15):440–444PubMedCrossRefGoogle Scholar
  60. Rasmussen TB, Bjarnsholt T, Skindersoe ME, Hentzer M, Kristoffersen P, Köte 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(5):1799–1814PubMedCrossRefGoogle Scholar
  61. Rasmussen TB, Skindersoe ME, Bjarnsholt T, Phipps RK, Christensen KB, Jensen PO, Anderson JB, Koch B, Larsen TO, Hentzer M, Eberl L, Høiby N, Givskov M (2005b) Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151(5):1325–1340PubMedCrossRefGoogle Scholar
  62. Rediers H, Rainey PB, Vanderleyden J, De Mot R (2005) Unravelling the secret lives of bacteria: use of in vivo expression technology and differential fluorescence induction promoter traps as tools for exploring niche-specific gene expression. Microbiol Mol Biol Rev 69(2):217–261PubMedCrossRefGoogle Scholar
  63. Rivault F, Liébert C, Burger A, Hoegy F, Abdallah MA, Schalk IJ, Mislin GL (2007) Synthesis of pyochelin-norfloxacin conjugates. Bioorg Med Chem Lett 17(3):640–644PubMedCrossRefGoogle Scholar
  64. Roos V, Klemm P (2006) Global gene expression profiling of the asymptomatic bacteriuria Escherichia coli strain 83972 in the human urinary tract. Infect Immun 74(6):3565–3575PubMedCrossRefGoogle Scholar
  65. Rumbaugh KP, Griswold JA, Iglewski BH, Hamood AN (1999) Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infect Immun 67(11):5854–5862PubMedGoogle Scholar
  66. Rumbaugh KP, Griswold JA, Hamood AN (2000) The role of quorum sensing in the in vivo virulence of Pseudomonas aeruginosa. Microb Infect 2(14):1721–1731CrossRefGoogle Scholar
  67. Saelinger CB, Snell K, Holder IA (1977) Experimental studies on the pathogenesis of infections due to Pseudomonas aeruginosa: direct evidence for toxin producing during Pseudomonas infection of burned skin tissues. J Infect Dis 136(4):555–561PubMedGoogle Scholar
  68. Salunkhe P, Topfer T, Buer J, Tümmler B (2005) Genome-wide transcriptional profiling of the steady-state response of Pseudomonas aeruginosa to hydrogen peroxide. J Bacteriol 187(8):2565–2572PubMedCrossRefGoogle Scholar
  69. Schaber JA, Triffo WJ, Suh SJ, Oliver JW, Hastert MC, Griswold JA, Auer M, Hamood AN, Rumbaugh KP (2007) Pseudomonas aeruginosa forms biofilms in acute infection independent of cell-to-cell signaling. Infect Immun 75(8):3715–3721PubMedCrossRefGoogle Scholar
  70. Schaible UE, Kaufmann SH (2004) Iron and microbial infection. Nat Rev Microbiol 2(12):946–953PubMedCrossRefGoogle Scholar
  71. 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(7):2066–2079PubMedCrossRefGoogle Scholar
  72. Schuster M, Hawkins AC, Harwood CS, Greenberg EP (2004) The Pseudomonas aeruginosa RpoS regulon and its relationship to quorum sensing. Mol Microbiol 51(4):973–985PubMedCrossRefGoogle Scholar
  73. Shen K, Sayeed S, Antalis P, Gladitz J et al (2006) Extensive genomic plasticity in Pseudomonas aeruginosa revealed by identification and distribution studies of novel genes among clinical isolates. Infect Immun 74(9):5272–5283PubMedCrossRefGoogle Scholar
  74. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407(6805):762–764PubMedCrossRefGoogle Scholar
  75. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman L, D’Argenio D, Miller S, Ramsey BW, Speert DP, Moskowitz SM, Burns JL, Kaul R, Olson MV (2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103(22):8487–8492PubMedCrossRefGoogle Scholar
  76. Smith RS, Iglewski BH (2003) Pseudomonas aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6(1):56–60PubMedCrossRefGoogle Scholar
  77. Son MS, Matthews WJ Jr, Kang Y, Nguyen DT, Hoang TT (2007) In Vivo Evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun 75(11):5313–5324PubMedCrossRefGoogle Scholar
  78. Stieritz DD, Holder IA (1975) Experimental studies of the pathogenesis of infections due to Pseudomonas aeruginosa: description of a burned mouse model. J Infect Dis 131(6):688–691PubMedGoogle Scholar
  79. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD et al (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406(6799):959–964PubMedCrossRefGoogle Scholar
  80. Takase H, Nitanai H, Hoshino K, Otani T (2000) Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect Immun 68(4):1834–1839PubMedCrossRefGoogle Scholar
  81. Tredget EE, Shankowsky HA, Rennie R, Burrell RE, Logsetty S (2004) Pseudomonas infections in the thermally injured patient. Burns 30(1):3–26PubMedCrossRefGoogle Scholar
  82. Vasil ML, Ochsner UA (1999) The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 34(3):399–413PubMedCrossRefGoogle Scholar
  83. Vasil ML (2003) DNA microarrays in analysis of quorum sensing: strengths and limitations. J. Bacteriol 185(7):2061–2065PubMedCrossRefGoogle Scholar
  84. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH (2003) Microarray Analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185(7):2080–2095PubMedCrossRefGoogle Scholar
  85. Waite RD, Papakonstantinopoulou A, Littler E, Curtis MA (2005) Transcriptome analysis of Pseudomonas aeruginosa growth: comparison of gene expression in planktonic cultures and developing and mature biofilms. J Bacteriol 187(18):6571–6576PubMedCrossRefGoogle Scholar
  86. Waite RD, Paccanaro A, Papakonstantinopoulou A, Hurst JM, Saqi M, Littler E, Curtis MA (2006) Clustering of Pseudomonas aeruginosa transcriptomes from planktonic cultures, developing and mature biofilms reveals distinct expression profiles. BMC Genom 7:162CrossRefGoogle Scholar
  87. Wang J, Mushegian A, Lory S, Jin S (1996a) Large-scale isolation of candidate virulence genes of Pseudomonas aeruginosa by in vivo selection. Proc Natl Acad Sci USA 93(19):10434–10439PubMedCrossRefGoogle Scholar
  88. Wang J, Lory S, Ramphal R, Jin S (1996b) Isolation and characterization of Pseudomonas aeruginosa genes inducible by respiratory mucus derived from cystic fibrosis patients. Mol Microbiol 22(5):1005–1012PubMedCrossRefGoogle Scholar
  89. Wiehlmann L, Wagner G, Cramer N, Siebert B, Gudowius P, Morales G, Köhler T, van Delden C, Weinel C, Slickers P, Tümmler B (2007) Population structure of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 104(19):8101–8106PubMedCrossRefGoogle Scholar
  90. Wolfgang MC, Lee VT, Gilmore ME, Lory S (2003) Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 4(2):253–263PubMedCrossRefGoogle Scholar
  91. Wolfgang MC, Jyot J, Goodman AL, Ramphal R, Lory S (2004) Pseudomonas aeruginosa regulates flagellin expression as part of a global response to airway fluid from cystic fibrosis patients. Proc Natl Acad Sci USA 101(17):6664–6668PubMedCrossRefGoogle Scholar
  92. Yang H, Matewish M, Loubens I, Storey DG, Lam JS, Jin S (2000) migA, a quorum-responsive gene of Pseudomonas aeruginosa, is highly expressed in the cystic fibrosis lung environment and modifies low-molecular-mass lipopolysaccharide. Microbiology 146(10):2509–2519PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Piotr Bielecki
    • 1
  • Justyna Glik
    • 2
  • Marek Kawecki
    • 2
  • Vítor A. P. Martins dos Santos
    • 1
  1. 1.Systems & Synthetic Biology Research Group, Helmholtz Centre for Infection ResearchBraunschweigGermany
  2. 2.Centre for Burn TreatmentSiemianowice SlaskiePoland

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