Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa

FEMS Microbiology Reviews

Volumn 33, Issue 2, 2009, Pages 279-294

  Gooderham, W James ^a   Hancock, Robert E W ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b #232 2259 Lower Mall Research Station   (Canada)

Author keywords

Antimicrobial resistance; Pseudomonas aeruginosa; Two component regulatory system; Virulence

Indexed keywords

AMIKACIN; KANAMYCIN; STREPTOMYCIN;

ANTIBIOTIC RESISTANCE; BACTERIAL VIRULENCE; CYSTIC FIBROSIS; ESCHERICHIA COLI; LUNG INFECTION; MICROARRAY ANALYSIS; NONHUMAN; PHENOTYPE; PSEUDOMONAS AERUGINOSA; REVIEW; SALMONELLA ENTERICA;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIGNAL TRANSDUCTION; VIRULENCE;

NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 60149108120     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2008.00135.x     Document Type: Review

References (112)

1. Bader MW, Sanowar S, Daley ME, Schneider AR, Cho U, Xu W, Klevit RE, Le Moual H Miller SI (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122 : 461 472.
2. Baker-Austin C, Wright MS, Stepanauskas R McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14 : 176 182.
3. Beckmann B, Brittnacher M, Ernst R, Mayer-Hamblett N, Miller SI Burns JL (2005) Use of phage display to identify potential Pseudomonas aeruginosa gene products relevant to early cystic fibrosis airway infections. Infect Immun 73 : 444 452.
4. Belete B, Lu H Wozniak DJ (2008) Pseudomonas aeruginosa AlgR regulates type IV pilus biosynthesis by activating transcription of the fimU-pilVWXY1Y2E operon. J Bacteriol 190 : 2023 2030.
5. Boyd JM (2000) Localization of the histidine kinase PilS to the poles of Pseudomonas aeruginosa and identification of a localization domain. Mol Microbiol 36 : 153 162.
6. Boyd JM Lory S (1996) Dual function of PilS during transcriptional activation of the Pseudomonas aeruginosa pilin subunit gene. J Bacteriol 178 : 831 839.
7. Breidenstein EB, Khaira BK, Wiegand I Hancock RE (in press) A complex ciprofloxacin resistome revealed by screening a Pseudomonas aeruginosa mutant library for altered susceptibility. Antimicrob Agents Chemotherapy, in press.
8. Brinkman FS, Macfarlane EL, Warrener P Hancock RE (2001) Evolutionary relationships among virulence-associated histidine kinases. Infect Immun 69 : 5207 5211.
9. Caille O, Rossier C Perron K (2007) A copper-activated two-component system interacts with zinc and imipenem resistance in Pseudomonas aeruginosa. J Bacteriol 189 : 4561 4568.
10. Carterson AJ, Morici LA, Jackson DW et al 2004) The transcriptional regulator AlgR controls cyanide production in Pseudomonas aeruginosa. J Bacteriol 186 : 6837 6844.
11. Chen YT, Chang HY, Lu CL Peng HL (2004) Evolutionary analysis of the two-component systems in Pseudomonas aeruginosa PAO1. J Mol Evol 59 : 725 737.
12. Chieda Y, Iiyama K, Yasunaga-Aoki C, Lee JM, Kusakabe T Shimizu S (2005) Pathogenicity of gacA mutant of Pseudomonas aeruginosa PA01 in the silkworm, Bombyx mori. FEMS Microbiol Lett 244 : 181 186.
13. Coleman FT, Mueschenborn S, Meluleni G, Ray C, Carey VJ, Vargas SO, Cannon CL, Ausubel FM Pier GB (2003) Hypersusceptibility of cystic fibrosis mice to chronic Pseudomonas aeruginosa oropharyngeal colonization and lung infection. Proc Natl Acad Sci USA 100 : 1949 1954.
14. Conejo MC, Garcia I, Martinez-Martinez L, Picabea L Pascual A (2003) Zinc eluted from siliconized latex urinary catheters decreases OprD expression, causing carbapenem resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47 : 2313 2315.
15. D'Argenio DA, Gallagher LA, Berg CA Manoil C (2001) Drosophila as a model host for Pseudomonas aeruginosa infection. J Bacteriol 183 : 1466 1471.
16. D'Argenio DA, Calfee MW, Rainey PB Pesci EC (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184 : 6481 6489.
17. Darzins A Russell MA (1997) Molecular genetic analysis of type-4 pilus biogenesis and twitching motility using Pseudomonas aeruginosa as a model system - a review. Gene 192 : 109 115.
18. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, Lory S Ramphal R (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50 : 809 824.
19. Davies JA, Harrison JJ, Marques LL, Foglia GR, Stremick CA, Storey DG, Turner RJ, Olson ME Ceri H (2007) The GacS sensor kinase controls phenotypic reversion of small colony variants isolated from biofilms of Pseudomonas aeruginosa PA14. FEMS Microbiol Ecol 59 : 32 46.
20. Dean CR, Neshat S Poole K (1996) PfeR, an enterobactin-responsive activator of ferric enterobactin receptor gene expression in Pseudomonas aeruginosa. J Bacteriol 178 : 5361 5369.
21. Deretic V Konyecsni WM (1989) Control of mucoidy in Pseudomonas aeruginosa: transcriptional regulation of algR and identification of the second regulatory gene, algQ. J Bacteriol 171 : 3680 3688.
22. Deretic V, Dikshit R, Konyecsni WM, Chakrabarty AM Misra TK (1989) The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J Bacteriol 171 : 1278 1283.
23. Drenkard E Ausubel FM (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416 : 740 743.
24. Ernst RK, Yi EC, Guo L, Lim KB, Burns JL, Hackett M Miller SI (1999) Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286 : 1561 1565.
25. Falagas ME Bliziotis IA (2007) Pandrug-resistant Gram-negative bacteria: the dawn of the post-antibiotic era? Int J Antimicrob Agents 29 : 630 636.
26. Filloux A, Bally M, Soscia C, Murgier M Lazdunski A (1988) Phosphate regulation in Pseudomonas aeruginosa: cloning of the alkaline phosphatase gene and identification of phoB- and phoR-like genes. Mol Gen Genet 212 : 510 513.
27. Fridkin SK, Steward CD, Edwards JR et al 1999) Surveillance of antimicrobial use and antimicrobial resistance in United States hospitals: project ICARE phase 2. Project Intensive Care Antimicrobial Resistance Epidemiology (ICARE) hospitals. Clin Infect Dis 29 : 245 252.
28. Furukawa S, Kuchma SL O'Toole GA (2006) Keeping their options open: acute versus persistent infections. J Bacteriol 188 : 1211 1217.
29. Gallagher LA Manoil C (2001) Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183 : 6207 6214.
30. Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188 : 4169 4182.
31. Goldberg JB Dahnke T (1992) Pseudomonas aeruginosa AlgB, which modulates the expression of alginate, is a member of the NtrC subclass of prokaryotic regulators. Mol Microbiol 6 : 59 66.
32. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS Lory S (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7 : 745 754.
33. Hancock RE Speert DP (2000) Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat 3 : 247 255.
34. Hancock RE, Raffle VJ Nicas TI (1981) Involvement of the outer membrane in gentamicin and streptomycin uptake and killing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 19 : 777 785.
35. Hassan MT, van der Lelie D, Springael D, Romling U, Ahmed N Mergeay M (1999) Identification of a gene cluster, czr, involved in cadmium and zinc resistance in Pseudomonas aeruginosa. Gene 238 : 417 425.
36. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, Camara M, Williams P Haas D (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186 : 2936 2945.
37. Hickman JW, Tifrea DF Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102 : 14422 14427.
38. Hobbs M, Collie ES, Free PD, Livingston SP Mattick JS (1993) PilS and PilR, a two-component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol 7 : 669 682.
39. Hsu JL, Chen HC, Peng HL Chang HY (2008) Characterization of the histidine-containing phosphotransfer protein B-mediated multi-step phosphorelay system in Pseudomonas aeruginosa PAO1. J Biol Chem 283 : 9933 9944.
40. Huang B, Whitchurch CB Mattick JS (2003) FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa. J Bacteriol 185 : 7068 7076.
41. Ishimoto KS Lory S (1992) Identification of pilR, which encodes a transcriptional activator of the Pseudomonas aeruginosa pilin gene. J Bacteriol 174 : 3514 3521.
42. Jander G, Rahme LG Ausubel FM (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182 : 3843 3845.
43. Jensen V, Lons D, Zaoui C, Bredenbruch F, Meissner A, Dieterich G, Munch R Haussler S (2006) RhlR expression in Pseudomonas aeruginosa is modulated by the Pseudomonas quinolone signal via PhoB-dependent and -independent pathways. J Bacteriol 188 : 8601 8606.
44. Kay E, Humair B, Denervaud V, Riedel K, Spahr S, Eberl L, Valverde C Haas D (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188 : 6026 6033.
45. Kazmierczak BI, Lebron MB Murray TS (2006) Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol 60 : 1026 1043.
46. Kirisits MJ Parsek MR (2006) Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? Cell Microbiol 8 : 1841 1849.
47. Kuchma SL, Connolly JP O'Toole GA (2005) A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J Bacteriol 187 : 1441 1454.
48. Kulasakara H, Lee V, Brencic A et al 2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103 : 2839 2844.
49. Kulasekara HD, Ventre I, Kulasekara BR, Lazdunski A, Filloux A Lory S (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55 : 368 380.
50. Kwon DH Lu CD (2006) Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 50 : 1615 1622.
51. Kwon DH Lu CD (2007) Polyamine effects on antibiotic susceptibility in bacteria. Antimicrob Agents Chemother 51 : 2070 2077.
52. Labaer J, Qiu Q, Anumanthan A et al 2004) The Pseudomonas aeruginosa PA01 gene collection. Genome Res 14 : 2190 2200.
53. Lapouge K, Schubert M, Allain FH Haas D (2008) Gac/Rsm signal transduction pathway of Gammaproteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67 : 241 253.
54. Laskowski MA Kazmierczak BI (2006) Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect Immun 74 : 4462 4473.
55. Laskowski MA, Osborn E Kazmierczak BI (2004) A novel sensor kinase-response regulator hybrid regulates type III secretion and is required for virulence in Pseudomonas aeruginosa. Mol Microbiol 54 : 1090 1103.
56. Laub MT Goulian M (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41 : 121 145.
57. Leech AJ Mattick JS (2006) Effect of site-specific mutations in different phosphotransfer domains of the chemosensory protein ChpA on Pseudomonas aeruginosa motility. J Bacteriol 188 : 8479 8486.
58. Leech AJ, Sprinkle A, Wood L, Wozniak DJ Ohman DE (2008) The NtrC family regulator AlgB, which controls alginate biosynthesis in mucoid Pseudomonas aeruginosa, binds directly to the algD promoter. J Bacteriol 190 : 581 589.
59. Lewenza S, Falsafi RK, Winsor G, Gooderham WJ, McPhee JB, Brinkman FS Hancock RE (2005) Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: a tool for identifying differentially regulated genes. Genome Res 15 : 583 589.
60. Linares JF, Gustafsson I, Baquero F Martinez JL (2006) Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA 103 : 19484 19489.
61. Lizewski SE, Lundberg DS Schurr MJ (2002) The transcriptional regulator AlgR is essential for Pseudomonas aeruginosa pathogenesis. Infect Immun 70 : 6083 6093.
62. Ma S, Wozniak DJ Ohman DE (1997) Identification of the histidine protein kinase KinB in Pseudomonas aeruginosa and its phosphorylation of the alginate regulator algB. J Biol Chem 272 : 17952 17960.
63. Ma S, Selvaraj U, Ohman DE, Quarless R, Hassett DJ Wozniak DJ (1998) Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa. J Bacteriol 180 : 956 968.
64. Macfarlane EL, Kwasnicka A, Ochs MM Hancock RE (1999) PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol Microbiol 34 : 305 316.
65. Macfarlane EL, Kwasnicka A Hancock RE (2000) Role of Pseudomonas aeruginosa PhoP-PhoQ in resistance to antimicrobial cationic peptides and aminoglycosides. Microbiology 146 : 2543 2554.
66. Mahajan-Miklos S, Tan MW, Rahme LG Ausubel FM (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96 : 47 56.
67. Marr AK, Gooderham WJ Hancock RE (2006) Antibacterial peptides for therapeutic use: obstacles and realistic outlook. Curr Opin Pharmacol 6 : 468 472.
68. Mascher T, Helmann JD Unden G (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70 : 910 938.
69. McPhee JB, Lewenza S Hancock RE (2003) Cationic antimicrobial peptides activate a two-component regulatory system, PmrA-PmrB, that regulates resistance to polymyxin B and cationic antimicrobial peptides in Pseudomonas aeruginosa. Mol Microbiol 50 : 205 217.
70. 2+-induced gene regulation in Pseudomonas aeruginosa. J Bacteriol 188 : 3995 4006.
71. Morici LA, Carterson AJ, Wagner VE, Frisk A, Schurr JR, Honer zu Bentrup K, Hassett DJ, Iglewski BH, Sauer K Schurr MJ (2007) Pseudomonas aeruginosa AlgR represses the Rhl quorum-sensing system in a biofilm-specific manner. J Bacteriol 189 : 7752 7764.
72. Moskowitz SM, Ernst RK Miller SI (2004) PmrAB, a two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J Bacteriol 186 : 575 579.
73. Mougous JD, Cuff ME, Raunser S et al 2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 : 1526 1530.
74. O'Toole GA Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30 : 295 304.
75. Overhage J, Lewenza S, Marr AK Hancock RE (2007) Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 189 : 2164 2169.
76. Overhage J, Bains M, Brazas MD Hancock RE (2008) Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J Bacteriol 190 : 2671 2679.
77. Palmer KL, Mashburn LM, Singh PK Whiteley M (2005) Cystic fibrosis sputum supports growth and cues key aspects of Pseudomonas aeruginosa physiology. J Bacteriol 187 : 5267 5277.
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 1226.
79. Perron K, Caille O, Rossier C, Van Delden C, Dumas JL Kohler T (2004) CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J Biol Chem 279 : 8761 8768.
80. Pessi G, Williams F, Hindle Z, Heurlier K, Holden MT, Camara M, Haas D Williams P (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183 : 6676 6683.
81. Potvin E, Lehoux DE, Kukavica-Ibrulj I, Richard KL, Sanschagrin F, Lau GW Levesque RC (2003) In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol 5 : 1294 1308.
82. Rahme LG, Tan MW, Le L, Wong SM, Tompkins RG, Calderwood SB Ausubel FM (1997) Use of model plant hosts to identify Pseudomonas aeruginosa virulence factors. Proc Natl Acad Sci USA 94 : 13245 13250.
83. Rahme LG, Ausubel FM, Cao H et al 2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci USA 97 : 8815 8821.
84. Ramsey MM Whiteley M (2004) Pseudomonas aeruginosa attachment and biofilm development in dynamic environments. Mol Microbiol 53 : 1075 1087.
85. Reimmann C, Beyeler M, Latifi A, Winteler H, Foglino M, Lazdunski A Haas D (1997) The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol Microbiol 24 : 309 319.
86. Rietsch A, Wolfgang MC Mekalanos JJ (2004) Effect of metabolic imbalance on expression of type III secretion genes in Pseudomonas aeruginosa. Infect Immun 72 : 1383 1390.
87. Ritchings BW, Almira EC, Lory S Ramphal R (1995) Cloning and phenotypic characterization of fleS and fleR, new response regulators of Pseudomonas aeruginosa which regulate motility and adhesion to mucin. Infect Immun 63 : 4868 4876.
88. Rodrigue A, Quentin Y, Lazdunski A, Mejean V Foglino M (2000) Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8 : 498 504.
89. Ruer S, Stender S, Filloux A de Bentzmann S (2007) Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J Bacteriol 189 : 3547 3555.
90. 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 : 762 764.
91. Smith EE, Buckley DG, Wu Z et al 2006) Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 103 : 8487 8492.
92. Soscia C, Hachani A, Bernadac A, Filloux A Bleves S (2007) Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J Bacteriol 189 : 3124 3132.
93. Stephenson K Hoch JA (2002) Two-component and phosphorelay signal-transduction systems as therapeutic targets. Curr Opin Pharmacol 2 : 507 512.
94. Stock AM, Robinson VL Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69 : 183 215.
95. Stover CK, Pham XQ, Erwin AL et al 2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406 : 959 964.
96. Tan MW, Rahme LG, Sternberg JA, Tompkins RG Ausubel FM (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci USA 96 : 2408 2413.
97. Teitzel GM, Geddie A, De Long SK, Kirisits MJ, Whiteley M Parsek MR (2006) Survival and growth in the presence of elevated copper: transcriptional profiling of copper-stressed Pseudomonas aeruginosa. J Bacteriol 188 : 7242 7256.
98. Van Alst NE, Picardo KF, Iglewski BH Haidaris CG (2007) Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect Immun 75 : 3780 3790.
99. Vasil ML Ochsner UA (1999) The response of Pseudomonas aeruginosa to iron: genetics, biochemistry, and virulence. Mol Microbiol 34 : 399 413.
100. Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C, Molin S, Bleves S, Lazdunski A, Lory S Filloux A (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 103 : 171 176.
101. Venturi V (2006) Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30 : 274 291.
102. Wagner VE, Li LL, Isabella VM Iglewski BH (2007) Analysis of the hierarchy of quorum-sensing regulation in Pseudomonas aeruginosa. Anal Bioanal Chem 387 : 469 479.
103. Wang Y, Ha U, Zeng L Jin S (2003) Regulation of membrane permeability by a two-component regulatory system in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47 : 95 101.
104. Whitchurch CB, Alm RA Mattick JS (1996) The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 93 : 9839 9843.
105. Whitchurch CB, Erova TE, Emery JA, Sargent JL, Harris JM, Semmler AB, Young MD, Mattick JS Wozniak DJ (2002) Phosphorylation of the Pseudomonas aeruginosa response regulator AlgR is essential for type IV fimbria-mediated twitching motility. J Bacteriol 184 : 4544 4554.
106. Whitchurch CB, Leech AJ, Young MD et al 2004) Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa. Mol Microbiol 52 : 873 893.
107. 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 : 253 263.
108. Wood LF, Leech AJ Ohman DE (2006) Cell wall-inhibitory antibiotics activate the alginate biosynthesis operon in Pseudomonas aeruginosa: roles of sigma (AlgT) and the AlgW and Prc proteases. Mol Microbiol 62 : 412 426.
109. Wozniak DJ Ohman DE (1991) Pseudomonas aeruginosa AlgB, a two-component response regulator of the NtrC family, is required for algD transcription. J Bacteriol 173 : 1406 1413.
110. Wu W, Badrane H, Arora S, Baker HV Jin S (2004) MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J Bacteriol 186 : 7575 7585.
111. Yahr TL Wolfgang MC (2006) Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol Microbiol 62 : 631 640.
112. Yu H, Mudd M, Boucher JC, Schurr MJ Deretic V (1997) Identification of the algZ gene upstream of the response regulator algR and its participation in control of alginate production in Pseudomonas aeruginosa. J Bacteriol 179 : 187 193.