Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication

Molecular Microbiology

Volumn 50, Issue 5, 2003, Pages 1477-1491

  Duan, Kangmin ^a   Dammel, Carol ^b   Stein, Jeffrey ^b   Rabin, Harvey ^a   Surette, Michael G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b Quorex Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOINDUCER 2 MEDIATED QUORUM SENSING; BACTERIAL GENOME; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM TRANSDUCTION; CELL COMMUNICATION; CELL INTERACTION; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PATTERN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INDUCTION; HOST PATHOGEN INTERACTION; IN VITRO STUDY; INTERSPECIES COMMUNICATION; LUNG INFECTION; LUNG INJURY; MICROFLORA; MOUTH FLORA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PSEUDOMONAS AERUGINOSA; RAT; SIGNAL TRANSDUCTION; SPUTUM;

ANIMALS; BACTERIAL PROTEINS; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, BACTERIAL; HOMOSERINE; HUMANS; LACTONES; LUNG; OROPHARYNX; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RATS; SIGNAL TRANSDUCTION; SPUTUM; STAPHYLOCOCCUS; STREPTOCOCCUS; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0346887122     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03803.x     Document Type: Article

References (79)

1. Akrim, M., Bally, M., Ball, G., Tommassen, J., Teerink, H., Filloux, A., and Lazdunski, A. (1993) Xcp-mediated protein secretion in Pseudomonas aeruginosa: identification of two additional genes and evidence for regulation of xcp gene expression. Mol Microbiol 10: 431-443.
2. Bals, R., Weiner, D.J., and Wilson, J.M. (1999) The innate immune system in cystic fibrosis lung disease. J Clin Invest 103: 303-307.
3. Bassler, B.L. (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2: 582-587.
4. Bassler, B.L., Wright, M., and Silverman, M.R. (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 13: 273-286.
5. Belanger, M., Burrows, L.L., and Lam, J.S. (1999) Functional analysis of genes responsible for the synthesis of the B-band O antigen of Pseudomonas aeruginosa serotype O6 lipopolysaccharide. Microbiology 145: 3505-3521.
6. Bever, R.A., and Iglewski, B.H. (1988) Molecular characterization and nucleotide sequence of the Pseudomonas aeruginosa elastase structural gene. J Bacteriol 170: 4309-4314.
7. Bjarnason, J., Southward, C., and Surette, M.G. (2003) Genomic profiling of iron-responsive genes in Salmonella by high throughput screening of a random promoter library. J Bacteriol 185: 4973-4982.
8. Brimer, C.D., and Montie, T.C. (1998) Cloning and comparison of fliC genes and identification of glycosylation in the flagellin of Pseudomonas aeruginosa a-type strains. J Bacteriol 180: 3209-3217.
9. Brint, J.M., and Ohman, D.E. (1995) Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhIR-RhII, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 177: 7155-7163.
10. Brown, N.L., Ford, S.J., Pridmore, R.D., and Fritzinger, D.C. (1983) Nucleotide sequence of a gene from the Pseudomonas transposon Tn501 encoding mercuric reductase. Biochemistry 22: 4089-4095.
11. Cash, H.A., Woods, D.E., McCullough, B., Johanson, W.G., Jr, and Bass, J.A. (1979) A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis 119: 453-459.
12. Chung, Y.J., and Saier, M.H., Jr (2002) Overexpression of the Escherichia coli sugE gene confers resistance to a narrow range of quaternary ammonium compounds. J Bacteriol 184: 2543-2545.
13. Coenye, T., Goris, J., Spilker, T., Vandamme, P., and LiPuma, J.J. (2002) Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinus limosus gen. nov., sp. nov. J Clin Microbiol 40: 2062-2069.
14. Cotter, P.A., and DiRita, V.J. (2000) Bacterial virulence gene regulation: an evolutionary perspective. Annu Rev Microbiol 54: 519-565.
15. Dekkers, L.C., Bloemendaal, C.J., de Weger, L.A., Wijffelman, C.A., Spaink, H.P., and Lugtenberg, B.J. (1998) A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365. Mol Plant-Microbe Interact 11: 45-56.
16. DeLisa, M.P., Wu, C.F., Wang, L., Valdes, J.J., and Bentley, W.E. (2001) DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 183: 5239-5247.
17. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
18. Erickson, D.L., Endersby, R., Kirkham, A., Stuber, K., Vollman, D.D., Rabin, H.R., et al. (2002) Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect Immun 70: 1783-1790.
19. Essar, D.W., Eberly, L., Hadero, A., and Crawford, I.P. (1990) Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol 172: 884-900.
20. Falk, P.G., Hooper, L.V., Midtvedt, T., and Gordon, J.I. (1998) Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol Mol Biol Rev 62: 1157-1170.
21. Favre-Bonte, S., Pache, J.C., Robert, J., Blanc, D., Pechere, J.C., and van Delden, C. (2002) Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients. Microb Pathog 32: 143-147.
22. Feldman, M., Bryan, R., Rajan, S., Scheffler, L., Brunnert, S., Tang, H., and Prince, A. (1998) Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51.
23. Folders, J., Tommassen, J., van Loon, L.C., and Bitter, W. (2000) Identification of a chitin-binding protein secreted by Pseudomonas aeruginosa. J Bacteriol 182: 1257-1263.
24. Fong, K.P., Chung, W.O., Lamont, R.J., and Demuth, D.R. (2001) Intra-and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect Immun 69: 7625-7634.
25. Fuqua, C., Parsek, M.R., and Greenberg, E.P. (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35: 439-468.
26. Gray, G.L., Smith, D.H., Baldridge, J.S., Harkins, R.N., Vasil, M.L., Chen, E.Y., and Heyneker, H.L. (1984) Cloning, nucleotide sequence, and expression in Escherichia coli of the exotoxin A structural gene of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 81: 2645-2649.
27. Greenberg, E.P., Hastings, J.W., and Ulitzer, S. (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120: 87-91.
28. Guarner, F., and Malagelada, J.R. (2003) Gut flora in health and disease. Lancet 361: 512-519.
29. Hardegger, M., Koch, A.K., Ochsner, U.A., Fiechter, A., and Reiser, J. (1994) Cloning and heterologous expression of a gene encoding an alkane-induced extracellular protein involved in alkane assimilation from Pseudomonas aeruginosa. Appl Environ Microbiol 60: 3679-3687.
30. Hart, C.A., and Winstanley, C. (2002) Persistent and aggressive bacteria in the lungs of cystic fibrosis children. Br Med Bull 61: 81-96.
31. Hirakata, Y., Srikumar, R., Poole, K., Gotoh, N., Suematsu, T., Kohno, S., et al. (2002) Multidrug efflux systems play an important role in the invasiveness of Pseudomonas aeruginosa. J Exp Med 196: 109-118.
32. Holloway, B.W. (1955) Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13: 572-581.
33. Jaffar-Bandjee, M.C., Lazdunski, A., Bally, M., Carrere, J., Chazalette, J.P., and Galabert, C. (1995) Production of elastase, exotoxin A, and alkaline protease in sputa during pulmonary exacerbation of cystic fibrosis in patients chronically infected by Pseudomonas aeruginosa. J Clin Microbiol 33: 924-929.
34. Jann, A., Cavard, D., Martin, C., Cami, B., and Patte, J.C. (1990) A lipopeptide-encoding sequence upstream from the lysA gene of Pseudomonas aeruginosa. Mol Microbiol 4: 677-682.
35. Kulich, S.M., Yahr, T.L., Mende-Mueller, L.M., Barbieri, J.T., and Frank, D.W. (1994) Cloning the structural gene for the 49-kDa form of exoenzyme S (exoS) from Pseudomonas aeruginosa strain 388. J Biol Chem 269: 10431-10437.
36. Kuroda, A., Kumano, T., Taguchi, K., Nikata, T., Kato, J., and Ohtake, H. (1995) Molecular cloning and characterization of a chemotactic transducer gene in Pseudomonas aeruginosa. J Bacteriol 177: 7019-7025.
37. Latifi, A., Winson, M.K., Foglino, M., Bycroft, B.W., Stewart, G.S., Lazdunski, A., and Williams, P. (1995) Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol 17: 333-343.
38. Liang, X., Pham, X.Q., Olson, M.V., and Lory, S. (2001) Identification of a genomic island present in the majority of pathogenic isolates of Pseudomonas aeruginosa. J Bacteriol 183: 843-853.
39. Lyon, W.R., Madden, J.C., Levin, J.C., Stein, J.L., and Caparon, M.G. (2001) Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42: 145-157.
40. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
41. McNab, R., Ford, S.K., El-Sabaeny, A., Barbieri, B., Cook, G.S., and Lamont, R.J. (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185: 274-284.
42. Mavrodi, D.V., Bonsall, R.F., Delaney, S.M., Soule, M.J., Phillips, G., and Thomashow, L.S. (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183: 6454-6465.
43. Middleton, B., Rodgers, H.C., Camara, M., Knox, A.J., Williams, P., and Hardman, A. (2002) Direct detection of N-acylhomoserine lactones in cystic fibrosis sputum. FEMS Microbiol Lett 207: 1-7.
44. Miller, M.B., and Bassler, B.L. (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
45. Miller, M.B., Skorupski, K., Lenz, D.H., Taylor, R.K., and Bassler, B.L. (2002) Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110: 303-314.
46. Murray, P.R. (1995) Manual of Clinical Microbiology. Washington, DC: American Society for Microbiology Press.
47. Ochsner, U.A., and Reiser, J. (1995) Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92: 6424-6428.
48. Ochsner, U.A., Fiechter, A., and Reiser, J. (1994) Isolation, characterization, and expression in Escherichia coli of the Pseudomonas aeruginosa rhIAB genes encoding a rhamnosyltransferase involved in rhamnolipid biosurfactant synthesis. J Biol Chem 269: 19787-19795.
49. Ohtani, K., Hayashi, H., and Shimizu, T. (2002) The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol Microbiol 44: 171-179.
50. Passador, L., Cook, J.M., Gambello, M.J., Rust, L., and Iglewski, B.H. (1993) Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260: 1127-1130.
51. Peche're, J.-C. (2001) New perspectives on macrolide antibiotics. Int J Antimicrob Agents 18: S93-S97.
52. Pesci, E.G., Milbank, J.B., Pearson, J.P., McKnight, S., Kende, A.S., Greenberg, E.P., and Iglewski, B.H. (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96: 11229-11234.
53. Rajan, S., and Saiman, L. (2002) Pulmonary infections in patients with cystic fibrosis. Semin Respir Infect 17: 47-56.
54. Saiman, L. (2002) Do macrolides have an anti-inflammatory effect? In 16th Annual North American Cystic Fibrosis Conference, S124 New Orleans, Louisiana, October 3-6, 2002.
55. Schauder, S., Shokat, K., Surette, M.G., and Bassler, B.L. (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41: 463-476.
56. Schöni, M.H. (2003) Macrolide antibiotic therapy in patients with cystic fibrosis. Swiss Med Wkly 133: 297-301.
57. Schuster, M., Lostroh, C.P., Ogi, T., and Greenberg, E.P. (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185: 2066-2079.
58. Shreve, M.R., Butler, S., Kaplowitz, H.J., Rabin, H.R., Stokes, D., Light, M., and Regelmann, W.E. (1999) Impact of microbiology practice on cumulative prevalence of respiratory tract bacteria in patients with cystic fibrosis. J Clin Microbiol 37: 753-757.
59. Singh, P.K., Schaefer, A.L., Parsek, M.R., Moninger, T.O., Welsh, M.J., and Greenberg, E.P. (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407: 762-764.
60. Smith, R.S., and Iglewski, B.H. (2003) P. aeruginosa quorumsensing systems and virulence. Curr Opin Microbiol 6: 56-60.
61. Soni, R., Marks, G., Henry, D.A., Robinson, M., Moriarty, C., Parsons, S., et al. (2002) Effect of Burkholderia cepacia infection in the clinical course of patients with cystic fibrosis: a pilot study in a Sydney clinic. Respirology 7: 241-245.
62. Stevenson, B., and Babb, K. (2002) LuxS-mediated quorum sensing in Borrelia burgdorferi, the Lyme disease spirochete. Infect Immun 70: 4099-4105.
63. Stintzi, A., Johnson, Z., Stonehouse, M., Ochsner, U., Meyer, J.M., Vasil, M.L., and Poole, K. (1999) The pvc gene cluster of Pseudomonas aeruginosa: role in synthesis of the pyoverdine chromophore and regulation by PtxR and PvdS. J Bacteriol 181: 4118-4124.
64. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406: 959-964.
65. Sundin, G.W., Shankar, S., Chugani, S.A., Chopade, B.A., Kavanaugh-Black, A., and Chakrabarty, A.M. (1996) Nucleoside diphosphate kinase from Pseudomonas aeruginosa: characterization of the gene and its role in cellular growth and exopolysaccharide alginate synthesis. Mol Microbiol 20: 965-979.
66. Surette, M.G., and Bassler, B.L. (1998) Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc Natl Acad Sci USA 95: 7046-7050.
67. Surette, M.G., Miller, M.B., and Bassler, B.L. (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci USA 96: 1639-1644.
68. Tanaka, K., and Takahashi, H. (1994) Cloning, analysis and expression of an rpoS homologue gene from Pseudomonas aeruginosa PAO1. Gene 150: 81-85.
69. Tancrede, C. (1992) Role of human microflora in health and disease. Eur J Clin Microbiol Infect Dis 11: 1012-1015.
70. Wagner, V.E., Bushnell, D., Passador, L., Brooks, A.I., and Iglewski, B.H. (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185: 2080-2095.
71. West, S.E., Schweizer, H.P., Dall, C., Sample, A.K., and Runyen-Janecky, L.J. (1994) Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148: 81-86.
72. Whitehead, N.A., Barnard, A.M., Slater, H., Simpson, N.J., and Salmond, G.P. (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25: 365-404.
73. Winzer, K., Sun, Y.H., Green, A., Delory, M., Blackley, D., Hardie, K.R., et al. (2002) Role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteremic infection. Infect Immun 70: 2245-2248.
74. Wolter, J.M., Bowler, S.D., and McCormack, J.G. (1999) Are antipseudomonal antibiotics really beneficial in acute respiratory exacerbations of cystic fibrosis? Aust NZ J Med 29: 15-21.
75. Xavier, K.B., and Bassler, B.L. (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6: 191-197.
76. Yahr, T.L., Barbieri, J.T., and Frank, D.W. (1996) Genetic relationship between the 53-and 49-kilodalton forms of exoenzyme S from Pseudomonas aeruginosa. J Bacteriol 178: 1412-1419.
77. Yahr, T.L., Vallis, A.J., Hancock, M.K., Barbieri, J.T., and Frank, D.W. (1998) ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc Natl Acad Sci USA 95: 13899-13904.
78. Yoon, S.S., Hennigan, R.F., Hilliard, G.M., Ochsner, U.A., Parvatiyar, K., Kamani, M.C., et al. (2002) Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell 3: 593-603.
79. Zhu, J., Miller, M.B., Vance, R.E., Dziejman, M., Bassler, B.L., and Mekalanos, J.J. (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 99: 3129-3134.