Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family
10.1128/jb.177.24.7155-7163.1995
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Mutants of Pseudomonas aeruginosa PAO1 that were deficient in the ability to produce proteases that degrade casein were detected among the survivors of chemical mutagenesis. One such mutant (PDO31) showed reduced production of elastolytic activity, beta-hemolytic activity, and pyocyanin. A 4.3-kb EcoRI fragment from a gene bank of PAO1 that complemented defects in PDO31 was found. Transposon mutagenesis and deletion derivatives of the clone were used in conjunction with complementation tests to determine the physical location of the gene of interest. Nucleotide sequence analysis revealed an open reading frame (rhlR) encoding a putative 27.6-kDa protein (RhlR) with homology to autoinducer-responsive regulators of quorum sensing systems such as LuxR of Vibrio fischeri and LasR of P. aeruginosa. Further sequence analysis downstream of rhlR revealed an independently transcribed gene (rhlI) that encodes a putative 22.2-kDa protein with homology to members of the family of autoinducer synthetases, such as LuxI of V. fischeri and LasI of P. aeruginosa. The rhlRI sequences were also recently reported by others (U.A. Ochsner and J. Reiser, Proc. Natl. Acad. Sci. USA 92: 6424-6428, 1995) as an autoinducer-mediated regulation mechanism for rhamnolipid biosurfactant synthesis in P. aeruginosa PG201. Mutants with defects in rhlR or rhlI were constructed in PAO1 by gene replacement, using clones modified by Tn501 insertion. Compared with the wild type, the rhlR and rhlI mutants both showed defects in the production of elastase, LasA protease, rhamnolipid, and pyocyanin. Transcription from the gene for elastase, as measured with a lasB-cat fusion, demonstrated that production of elastase was subject to cell density-dependent gene activation in PAO1. However, transcription of lasB-cat in the rhlI mutant, which had lost the presumptive autoinducer synthetase (predicted to activate RhlR), showed low basal activity and had lost all cell density-dependent transcription of lasB. Thus, RhlR-RhlI represent the second autoinducer-responsive regulatory mechanism found in P. aeruginosa that controls expression of multiple virulence factor exoproducts, including elastase.

Bibliography

Brint, J. M., & Ohman, D. E. (1995). Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. Journal of Bacteriology, 177(24), 7155–7163.

Authors 2
  1. J M Brint (first)
  2. D E Ohman (additional)
References 65 Referenced 476
  1. Bainton , N. J. , B. W. Bycroft , S. R. Chhabra , P. Stead , L. Gledhill , P. J. Hill , C. E. D. Rees , M. K. Winson , G. P. C. Salmond , G. S. A. B. Stewart , and P. Williams . 1992 . A general role for the lux autoinducer in bacterial cell signaling: control of antibiotic synthesis in Erwinia . Gene 116 : 87 - 91 . (10.1016/0378-1119(92)90633-Z) / Gene / A general role for the lux autoinducer in bacterial cell signaling: control of antibiotic synthesis in Erwinia by Bainton N. J. (1992)
  2. Bassler , B. L. , M. Wright , and M. R. Silverman . 1994 . Multiple signalling systems controlling expression of Iuminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway . Mol. Microbiol. 13 : 273 - 286 . (10.1111/j.1365-2958.1994.tb00422.x) / Mol. Microbiol. / Multiple signalling systems controlling expression of Iuminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway by Bassler B. L. (1994)
  3. Blackwood , L. L. , R. M. Stone , B. H. Iglewski , and J. E. Pennington . 1983 . Evaluation of Pseudomonas aeruginosa exotoxin A and elastase as virulence factors in acute Iung infection . Infect. Immun. 39 : 198 - 201 . (10.1128/iai.39.1.198-201.1983) / Infect. Immun. / Evaluation of Pseudomonas aeruginosa exotoxin A and elastase as virulence factors in acute Iung infection by Blackwood L. L. (1983)
  4. Brint J. M. 1992. Pseudomonas aeruginosa lasM encodes a regulator of lasB transcription exoproduct synthesis and growth phase transition abstr. D49. In Abstracts of the 92nd Annual Meeting of the American Society for Microbiology 1992. American Society for Microbiology Washington D.C.
  5. Britigan , B. E. , T. L. Roeder , G. T. Rasmussen , D. M. Shasby , M. L. Mc-Cormick , and C. D. Cox . 1992 . Interaction of the Pseudomonas aeruginosa secretory products pyocyanin and pyochelin generates hydroxyl radicals and causes synergistic damage to endothelial cells . J. Clin. Invest. 90 : 2187 - 2196 . (10.1172/JCI116104) / J. Clin. Invest. / Interaction of the Pseudomonas aeruginosa secretory products pyocyanin and pyochelin generates hydroxyl radicals and causes synergistic damage to endothelial cells by Britigan B. E. (1992)
  6. Bryan , C. S. , and K. L. Reynolds . 1984 . Bacteremic nosocomial pneumonia-analysis of 172 episodes from a single metropolitan area . Am. Rev. Respir. Dis. 129 : 668 - 671 . (10.1164/arrd.1984.129.5.668) / Am. Rev. Respir. Dis. / Bacteremic nosocomial pneumonia-analysis of 172 episodes from a single metropolitan area by Bryan C. S. (1984)
  7. Cox , C. D. 1986 . Role of pyocyanin in the acquisition of iron from transferrin . Infect. Immun. 52 : 263 - 270 . (10.1128/iai.52.1.263-270.1986) / Infect. Immun. / Role of pyocyanin in the acquisition of iron from transferrin by Cox C. D. (1986)
  8. Cross , A. , J. R. Allen , J. Burke , G. Ducel , A. Harris , J. John , D. Johnson , M. Lew , B. MacMillan , R. Skalova , R. Wenzel , and J. Tenney . 1983 . Nosocomial infections due to Pseudomonas aeruginosa: review of recent trends . Rev. Infect. Dis. 5(Suppl. ): S837 - S845 . (10.1093/clinids/5.Supplement_5.S837) / Rev. Infect. Dis. / Nosocomial infections due to Pseudomonas aeruginosa: review of recent trends by Cross A. (1983)
  9. Crouch , S. , R. Wunderink , C. Jones , K. Leeper , and G. Meduri . 1993 . Mortality and cause of death in ventilator-associated pneumonia (VAP) due to Pseudomonas. Am. Rev. Respir. Dis. 147 : A99 . / Pseudomonas. Am. Rev. Respir. Dis. / Mortality and cause of death in ventilator-associated pneumonia (VAP) due to by Crouch S. (1993)
  10. Döring , G. , M. Maier , E. Muller , B. Zoubair , B. Tummler , and A. Kharazmi . 1987 . Virulence factors of Pseudomonas aeruginosa . Antibiot. Chemother. 39 : 136 - 148 . (10.1159/000414341) / Antibiot. Chemother. / Virulence factors of Pseudomonas aeruginosa by Döring G. (1987)
  11. Dunn , M. , and R. G. Wunderink . 1995 . Ventilator-associated pneumonia caused by Pseudomonas infection . Clin. Chest Med. 16 : 95 - 109 . (10.1016/S0272-5231(21)00980-1) / Clin. Chest Med. / Ventilator-associated pneumonia caused by Pseudomonas infection by Dunn M. (1995)
  12. Fagon , J. - Y. , J. Chastre , Y. Domart , J. -L. Trouillet , J. Pierre , C. Darne , and C. Gibert . 1989 . Nosocomial pneumonia in patients receiving continuous mechanical ventilation: prospective analysis of 52 episodes with use of a protected specimen brush and quantitative culture techniques . Am. Rev. Respir. Dis. 139 : 877 - 884 . (10.1164/ajrccm/139.4.877) / Am. Rev. Respir. Dis. / Nosocomial pneumonia in patients receiving continuous mechanical ventilation: prospective analysis of 52 episodes with use of a protected specimen brush and quantitative culture techniques by Fagon J. (1989)
  13. Fagon , J. - Y. , J. Chastre , A. J. Hance , P. Montravers , A. Norvara , and C. Gibert . 1993 . Nosocomial pneumonia in ventilated patients: a cohort study evaluating attributable mortality and hospital stay . Am. J. Med. 94 : 281 - 288 . (10.1016/0002-9343(93)90060-3) / Am. J. Med. / Nosocomial pneumonia in ventilated patients: a cohort study evaluating attributable mortality and hospital stay by Fagon J. (1993)
  14. Figurski , D. , and D. R. Helinski . 1979 . Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans . Proc. Natl. Acad. Sci. USA 76 : 1648 - 1652 . (10.1073/pnas.76.4.1648) / Proc. Natl. Acad. Sci. USA / Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans by Figurski D. (1979)
  15. Frank , D. W. , and B. H. Iglewski . 1991 . Cloning and sequence analysis of a trans-regulatory locus required for exoenzyme S synthesis in Pseudomonas aeruginosa . J. Bacteriol. 173 : 6460 - 6468 . (10.1128/jb.173.20.6460-6468.1991) / J. Bacteriol. / Cloning and sequence analysis of a trans-regulatory locus required for exoenzyme S synthesis in Pseudomonas aeruginosa by Frank D. W. (1991)
  16. Franklin , M. J. , C. E. Chitnis , P. Gacesa , A. Sonesson , D. C. White , and D. E. Ohman . 1994 . Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase . J. Bacteriol. 176 : 1821 - 1830 . (10.1128/jb.176.7.1821-1830.1994) / J. Bacteriol. / Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase by Franklin M. J. (1994)
  17. Friedman , A. M. , S. R. Long , S. E. Brown , W. J. Buikema , and F. M. Ausubel . 1982 . Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants . Gene 18 : 289 - 296 . (10.1016/0378-1119(82)90167-6) / Gene / Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants by Friedman A. M. (1982)
  18. Fuqua , W. C. , S. C. Winans , and E. P. Greenberg . 1994 . Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators . J. Bacteriol. 176 : 269 - 275 . (10.1128/jb.176.2.269-275.1994) / J. Bacteriol. / Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators by Fuqua W. C. (1994)
  19. Gambello , M. J. , and B. H. Iglewski . 1991 . Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression . J. Bacteriol. 173 : 3000 - 3009 . (10.1128/jb.173.9.3000-3009.1991) / J. Bacteriol. / Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression by Gambello M. J. (1991)
  20. Gambello , M. J. , S. Kaye , and B. H. Iglewski . 1993 . LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression . Infect. Immun. 61 : 1180 - 1184 . (10.1128/iai.61.4.1180-1184.1993) / Infect. Immun. / LasR of Pseudomonas aeruginosa is a transcriptional activator of the alkaline protease gene (apr) and an enhancer of exotoxin A expression by Gambello M. J. (1993)
  21. Goldberg , J. B. , and D. E. Ohman . 1984 . Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate . J. Bacteriol. 158 : 1115 - 1121 . (10.1128/jb.158.3.1115-1121.1984) / J. Bacteriol. / Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate by Goldberg J. B. (1984)
  22. Goldberg , J. B. , and D. E. Ohman . 1987 . Cloning and transcriptional regulation of the elastase lasA gene in mucoid and nonmucoid Pseudomonas aeruginosa . J. Bacteriol. 169 : 1349 - 1351 . (10.1128/jb.169.3.1349-1351.1987) / J. Bacteriol. / Cloning and transcriptional regulation of the elastase lasA gene in mucoid and nonmucoid Pseudomonas aeruginosa by Goldberg J. B. (1987)
  23. Govan , J. R. W. , and J. A. M. Fyfe . 1978 . Mucoid Pseudomonas aeruginosa and cystic fibrosis: resistance of the mucoid form to carbenicillin, flucloxacillin and tobramycin and the isolation of mucoid variants in vitro . J. Antimicrob. Chemother. 4 : 233 - 240 . (10.1093/jac/4.3.233) / J. Antimicrob. Chemother. / Mucoid Pseudomonas aeruginosa and cystic fibrosis: resistance of the mucoid form to carbenicillin, flucloxacillin and tobramycin and the isolation of mucoid variants in vitro by Govan J. R. W. (1978)
  24. Hingley , S. T. , A. T. Hastie , F. Kueppers , M. L. Higgins , G. Weinbuam , and T. Shrylock . 1986 . Effect of ciliostatic factors from Pseudomonas aeruginosa on rabbit respiratory cilia . Infect. Immun. 51 : 254 - 262 . (10.1128/iai.51.1.254-262.1986) / Infect. Immun. / Effect of ciliostatic factors from Pseudomonas aeruginosa on rabbit respiratory cilia by Hingley S. T. (1986)
  25. Holloway , B. W. 1969 . Genetics of Pseudomonas . Bacteriol. Rev. 33 : 419 - 443 . (10.1128/br.33.3.419-443.1969) / Bacteriol. Rev. / Genetics of Pseudomonas by Holloway B. W. (1969)
  26. Holloway , B. W. , and A. F. Morgan . 1986 . Genome organization in Pseudomonas. Annu. Rev. Microbiol. 40 : 79 - 105 . (10.1146/annurev.mi.40.100186.000455) / Pseudomonas. Annu. Rev. Microbiol. / Genome organization by Holloway B. W. (1986)
  27. Iannini , P. B. , T. Claffey , and R. Quintiliani . 1974 . Bacteremic pseudomonas pneumonia . JAMA 230 : 558 - 561 . (10.1001/jama.230.4.558) / JAMA / Bacteremic pseudomonas pneumonia by Iannini P. B. (1974)
  28. Jones , S. , B. Yu , N. J. Bainton , M. Birdsall , B. W. Bycroft , S. R. Chhabra , A. J. R. Cox , P. Golby , P. J. Reeves , S. Stephens , M. K. Winson , G. P. C. Salmond , G. S. A. B. Stewart , and P. Williams . 1993 . The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa . EMBO J. 12 : 2477 - 2482 . (10.1002/j.1460-2075.1993.tb05902.x) / EMBO J. / The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa by Jones S. (1993)
  29. Kessler , E. , M. Safrin , N. Landshman , A. Chechick , and S. Blumberg . 1982 . In vitro inhibition of Pseudomonas aeruginosa elastase by metal-chelating peptide derivatives . Infect. Immun. 38 : 716 - 723 . (10.1128/iai.38.2.716-723.1982) / Infect. Immun. / In vitro inhibition of Pseudomonas aeruginosa elastase by metal-chelating peptide derivatives by Kessler E. (1982)
  30. Kessler , E. , M. Safrin , J. C. Olson , and D. E. Ohman . 1993 . Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease . J. Biol. Chem. 268 : 7503 - 7508 . (10.1016/S0021-9258(18)53203-8) / J. Biol. Chem. / Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease by Kessler E. (1993)
  31. Kuo , A. , N. V. Blough , and P. V. Dunlap . 1994 . Multiple N-acyl-L-homoserine lactone autoinducers of Iuminescence in the marine symbiotic bacterium Vibrio fischeri . J. Bacteriol. 176 : 7558 - 7565 . (10.1128/jb.176.24.7558-7565.1994) / J. Bacteriol. / Multiple N-acyl-L-homoserine lactone autoinducers of Iuminescence in the marine symbiotic bacterium Vibrio fischeri by Kuo A. (1994)
  32. Laemmli , U. K. 1970 . Cleavage of structural proteins during the assembly of the head of bacteriophage T4 . Nature (London) 227 : 680 - 685 . (10.1038/227680a0) / Nature (London) / Cleavage of structural proteins during the assembly of the head of bacteriophage T4 by Laemmli U. K. (1970)
  33. Latifi , A. , M. K. Winson , M. Foglino , B. W. Bycroft , G. S. A. B. Stewart , A. Lazdunski , and P. Williams . 1995 . Multiple homologues of LuxR and LuxI control the expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1 . Mol. Microbiol. 17 : 333 - 343 . (10.1111/j.1365-2958.1995.mmi_17020333.x) / Mol. Microbiol. / Multiple homologues of LuxR and LuxI control the expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1 by Latifi A. (1995)
  34. Liu , P. V. 1974 . Extracellular toxins of Pseudomonas aeruginosa . J. Infect. Dis. 130(Suppl. ): S94 - S99 . (10.1093/infdis/130.Supplement.S94) / J. Infect. Dis. / Extracellular toxins of Pseudomonas aeruginosa by Liu P. V. (1974)
  35. Maniatis T. E. F. Fritsch and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  36. McClure , C. D. , and N. L. Schiller . 1992 . Effects of Pseudomonas aeruginosa rhamnolipids on human monocyte-derived macrophages . J. Leukocyte Biol. 51 : 97 - 102 . (10.1002/jlb.51.2.97) / J. Leukocyte Biol. / Effects of Pseudomonas aeruginosa rhamnolipids on human monocyte-derived macrophages by McClure C. D. (1992)
  37. McIver , K. S. , E. Kessler , and D. E. Ohman . 1991 . Substitution of active site His-223 in Pseudomonas aeruginosa elastase and expression of the mutated lasB alleles in Escherichia coli show evidence for autoproteolytic processing of proelastase . J. Bacteriol. 173 : 7781 - 7789 . (10.1128/jb.173.24.7781-7789.1991) / J. Bacteriol. / Substitution of active site His-223 in Pseudomonas aeruginosa elastase and expression of the mutated lasB alleles in Escherichia coli show evidence for autoproteolytic processing of proelastase by McIver K. S. (1991)
  38. McIver , K. S. , J. C. Olson , and D. E. Ohman . 1993 . Pseudomonas aeruginosa lasB1 mutants produce an elastase, substituted at active-site His-223, that is defective in activity, processing, and secretion . J. Bacteriol. 175 : 4008 - 4015 . (10.1128/jb.175.13.4008-4015.1993) / J. Bacteriol. / Pseudomonas aeruginosa lasB1 mutants produce an elastase, substituted at active-site His-223, that is defective in activity, processing, and secretion by McIver K. S. (1993)
  39. Meduri , G. U. , D. H. Beals , A. G. Maijub , and V. Baselski . 1991 . Protected bronchoalveolar lavage: a new bronchoscopic technique to retrieve uncontaminated distal airway secretions . Am. Rev. Respir. Dis. 143 : 855 - 864 . (10.1164/ajrccm/143.4_Pt_1.855) / Am. Rev. Respir. Dis. / Protected bronchoalveolar lavage: a new bronchoscopic technique to retrieve uncontaminated distal airway secretions by Meduri G. U. (1991)
  40. Meduri , G. U. , R. G. Wunderink , K. V. Leeper , C. B. Jones , E. Tolley , and G. Mayhall . 1994 . Causes of fever and pulmonary densities in patients with clinical manifestations of ventilator-associated pneumonia . Chest 106 : 221 - 235 . (10.1378/chest.106.1.221) / Chest / Causes of fever and pulmonary densities in patients with clinical manifestations of ventilator-associated pneumonia by Meduri G. U. (1994)
  41. Meighen , E. A. 1991 . Molecular biology of bacterial bioluminescence . Microbiol. Rev. 55 : 123 - 142 . (10.1128/mr.55.1.123-142.1991) / Microbiol. Rev. / Molecular biology of bacterial bioluminescence by Meighen E. A. (1991)
  42. Morihara K. and J. Y. Homma. 1985. Pseudomonas proteases p. 41-79. In I. A. Holder (ed.) Bacterial enzymes and virulence. CRC Press Inc. Boca Raton Fla. (10.1201/9781351070041-3)
  43. Ochsner , U. A. , A. Fiechter , and J. Reiser . 1994 . Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis . J. Biol. Chem. 269 : 19787 - 19795 . (10.1016/S0021-9258(17)32089-6) / J. Biol. Chem. / Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhlAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis by Ochsner U. A. (1994)
  44. Ochsner , U. A. , A. K. Koch , A. Fiechter , and J. Reiser . 1994 . Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa . J. Bacteriol. 176 : 2044 - 2054 . (10.1128/jb.176.7.2044-2054.1994) / J. Bacteriol. / Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa by Ochsner U. A. (1994)
  45. Ochsner , U. A. , and J. Reiser . 1995 . Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa . Proc. Natl. Acad. Sci. USA 92 : 6424 - 6428 . (10.1073/pnas.92.14.6424) / Proc. Natl. Acad. Sci. USA / Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa by Ochsner U. A. (1995)
  46. Ohman , D. E. , S. J. Cryz , and B. H. Iglewski . 1980 . Isolation and characterization of a Pseudomonas aeruginosa PAO mutant that produces altered elastase . J. Bacteriol. 142 : 836 - 842 . (10.1128/jb.142.3.836-842.1980) / J. Bacteriol. / Isolation and characterization of a Pseudomonas aeruginosa PAO mutant that produces altered elastase by Ohman D. E. (1980)
  47. Ohman , D. E. , J. C. Sadoff , and B. H. Iglewski . 1980 . Toxin A-deficient mutants of Pseudomonas aeruginosa PA103: isolation and characterization . Infect. Immun. 28 : 899 - 908 . (10.1128/iai.28.3.899-908.1980) / Infect. Immun. / Toxin A-deficient mutants of Pseudomonas aeruginosa PA103: isolation and characterization by Ohman D. E. (1980)
  48. Ohman , D. E. , M. A. West , J. L. Flynn , and J. B. Goldberg . 1985 . Method for gene replacement in Pseudomonas aeruginosa used in construction of recA mutants: recA-independent instability of alginate production . J. Bacteriol. 162 : 1068 - 1074 . (10.1128/jb.162.3.1068-1074.1985) / J. Bacteriol. / Method for gene replacement in Pseudomonas aeruginosa used in construction of recA mutants: recA-independent instability of alginate production by Ohman D. E. (1985)
  49. Olson , J. C. , and D. E. Ohman . 1992 . Efficient production and processing of elastase and LasA by Pseudomonas aeruginosa require zinc and calcium ions . J. Bacteriol. 174 : 4140 - 4147 . (10.1128/jb.174.12.4140-4147.1992) / J. Bacteriol. / Efficient production and processing of elastase and LasA by Pseudomonas aeruginosa require zinc and calcium ions by Olson J. C. (1992)
  50. Passador , L. , J. M. Cook , M. J. Gambello , L. Rust , and B. H. Iglewski . 1993 . Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication . Science 260 : 1127 - 1130 . (10.1126/science.8493556) / Science / Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication by Passador L. (1993)
  51. Pearson , J. P. , K. M. Gray , L. Passador , K. D. Tucker , A. Eberhard , B. H. Iglewski , and E. P. Greenberg . 1994 . Structure of the autoinducer required for the expression of Pseudomonas aeruginosa virulence genes . Proc. Natl. Acad. Sci. USA 91 : 197 - 201 . (10.1073/pnas.91.1.197) / Proc. Natl. Acad. Sci. USA / Structure of the autoinducer required for the expression of Pseudomonas aeruginosa virulence genes by Pearson J. P. (1994)
  52. Pearson , J. P. , L. Passador , B. H. Iglewski , and E. P. Greenberg . 1995 . A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa . Proc. Natl. Acad. Sci. USA 92 : 1490 - 1494 . (10.1073/pnas.92.5.1490) / Proc. Natl. Acad. Sci. USA / A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa by Pearson J. P. (1995)
  53. Reynolds , H. Y. , A. S. Levine , R. E. Wood , C. H. Zierdt , D. C. Dale , and J. E. Pennington . 1975 . Pseudomonas aeruginosa infections: persisting problems and current research to find new therapies . Ann. Intern. Med. 82 : 819 - 831 . (10.7326/0003-4819-82-6-819) / Ann. Intern. Med. / Pseudomonas aeruginosa infections: persisting problems and current research to find new therapies by Reynolds H. Y. (1975)
  54. Scheld , W. M. , and G. L. Mandell . 1991 . Nosocomial pneumonia: pathogenesis and recent advances in diagnosis and therapy . Rev. Infect. Dis. 13(Suppl 9 ): S743 - S751 . (10.1093/clinids/13.Supplement_9.S743) / Rev. Infect. Dis. / Nosocomial pneumonia: pathogenesis and recent advances in diagnosis and therapy by Scheld W. M. (1991)
  55. Shortridge , V. D. , M. L. Pato , A. I. Vasil , and M. L. Vasil . 1991 . Physical mapping of virulence-associated genes in Pseudomonas aeruginosa by transverse alternating-field electrophoresis . Infect. Immun. 59 : 3596 - 3603 . (10.1128/iai.59.10.3596-3603.1991) / Infect. Immun. / Physical mapping of virulence-associated genes in Pseudomonas aeruginosa by transverse alternating-field electrophoresis by Shortridge V. D. (1991)
  56. Swift , S. , M. K. Winson , P. F. Chan , N. J. Bainton , M. Birdsall , P. J. Reeves , C. E. D. Rees , S. R. Chhabra , P. J. Hill , J. P. Throup , B. W. Bycroft , G. P. C. Salmond , P. Williams , and G. S. A. B. Stewart . 1993 . A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria . Mol. Microbiol. 10 : 511 - 520 . (10.1111/j.1365-2958.1993.tb00923.x) / Mol. Microbiol. / A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria by Swift S. (1993)
  57. Todor , D. S. , M. J. Gambello , and B. H. Iglewski . 1991 . Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR . Mol. Microbiol. 5 : 2003 - 2010 . (10.1111/j.1365-2958.1991.tb00822.x) / Mol. Microbiol. / Pseudomonas aeruginosa LasA: a second elastase under the transcriptional control of lasR by Todor D. S. (1991)
  58. Vogel , H. J. , and D. M. Bonner . 1956 . Acetylornithinase in Escherichia coli: partial purification and some properties . J. Biol. Chem. 218 : 97 - 106 . (10.1016/S0021-9258(18)65874-0) / J. Biol. Chem. / Acetylornithinase in Escherichia coli: partial purification and some properties by Vogel H. J. (1956)
  59. West , S. E. H. , A. K. Sample , and L. J. Runyen-Janecky . 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 : 7532 - 7542 . (10.1128/jb.176.24.7532-7542.1994) / J. Bacteriol. / The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family by West S. E. H. (1994)
  60. Wilson , R. , T. Pitt , G. Taylor , D. Watson , J. MacDermot , D. Sykes , D. Roberts , and P. Cole . 1987 . Pyocyanin and 1-hydroxyphenazine produced by Pseudomonas aeruginosa inhibit the beating of human respiratory cilia in vitro . J. Clin. Invest. 79 : 221 - 229 . (10.1172/JCI112787) / J. Clin. Invest. / Pyocyanin and 1-hydroxyphenazine produced by Pseudomonas aeruginosa inhibit the beating of human respiratory cilia in vitro by Wilson R. (1987)
  61. Woods , D. E. , W. S. Hwang , M. S. Shahrabadi , and J. U. Que . 1988 . Alteration of pulmonary structure by Pseudomonas aeruginosa exoenzyme S . J. Med. Microbiol. 26 : 133 - 141 . (10.1099/00222615-26-2-133) / J. Med. Microbiol. / Alteration of pulmonary structure by Pseudomonas aeruginosa exoenzyme S by Woods D. E. (1988)
  62. Woods , S. E. , S. J. Cryz , R. L. Friedman , and B. H. Iglewski . 1982 . Contribution of toxin A and elastase to virulence of Pseudomonas aeruginosa in chronic Iung infections of rats . Infect. Immun. 36 : 1223 - 1228 . (10.1128/iai.36.3.1223-1228.1982) / Infect. Immun. / Contribution of toxin A and elastase to virulence of Pseudomonas aeruginosa in chronic Iung infections of rats by Woods S. E. (1982)
  63. Wozniak , D. J. , and D. E. Ohman . 1991 . Pseudomonas aeruginosa AlgB, a two-component response regulator of the NtrC family, is required for algD transcription . J. Bacteriol. 173 : 1406 - 1413 . (10.1128/jb.173.4.1406-1413.1991) / J. Bacteriol. / Pseudomonas aeruginosa AlgB, a two-component response regulator of the NtrC family, is required for algD transcription by Wozniak D. J. (1991)
  64. Wozniak , D. J. , and D. E. Ohman . 1994 . Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT . J. Bacteriol. 176 : 6007 - 6014 . (10.1128/jb.176.19.6007-6014.1994) / J. Bacteriol. / Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT by Wozniak D. J. (1994)
  65. Zhao , G. , T. Xia , R. S. Fischer , and R. A. Jensen . 1992 . Cyclohexadienyl dehydratase from Pseudomonas aeruginosa-molecular cloning of the gene and characterization of the gene product . J. Biol. Chem. 267 : 2487 - 2493 . (10.1016/S0021-9258(18)45905-4) / J. Biol. Chem. / Cyclohexadienyl dehydratase from Pseudomonas aeruginosa-molecular cloning of the gene and characterization of the gene product by Zhao G. (1992)
Dates
Type When
Created 8 years, 9 months ago (Nov. 9, 2016, 9:22 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:54 p.m.)
Indexed 4 weeks, 2 days ago (Aug. 6, 2025, 8:37 a.m.)
Issued 29 years, 9 months ago (Dec. 1, 1995)
Published 29 years, 9 months ago (Dec. 1, 1995)
Published Print 29 years, 9 months ago (Dec. 1, 1995)
Funders 0

None

@article{Brint_1995, title={Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family}, volume={177}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.177.24.7155-7163.1995}, DOI={10.1128/jb.177.24.7155-7163.1995}, number={24}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Brint, J M and Ohman, D E}, year={1995}, month=dec, pages={7155–7163} }