Pseudomonas aeruginosa fimL regulates multiple virulence functions by intersecting with Vfr-modulated pathways

Molecular Microbiology

Volumn 55, Issue 5, 2005, Pages 1357-1378

  Whitchurch, Cynthia B ^a,b,e   Beatson, Scott A ^b,c,f   Comolli, James C ^a,g   Jakobsen, Thania ^a   Sargent, Jennifer L ^a   Bertrand, Jacob J ^a   West, Joyce ^a   Klausen, Mikkel ^d   Waite, Leslie L ^a   Kang, Pil Jung ^a,h   Tolker Nielsen, Tim ^d   Mattick, John S ^b,c   Engel, Joanne N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Australian Government Australian Research Council   (Australia)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e MONASH UNIVERSITY   (Australia)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^g ETHICON INC   (United States)

^h OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GLUTAMINE; HISTIDINE; THREONINE; VIRULENCE FACTOR;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BACTERIUM PILUS; BIOFILM; BIOSENSOR; CELL DAMAGE; CELL MOTILITY; CONTROLLED STUDY; CYTOLYSIS; CYTOPATHOGENIC EFFECT; DELETION MUTANT; FIML GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INSERTION; GENE LOSS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SUPPRESSOR GENE; WILD TYPE;

BACTERIAL PROTEINS; CYCLIC AMP; CYCLIC AMP RECEPTOR PROTEIN; EPITHELIAL CELLS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; OPERON; PSEUDOMONAS AERUGINOSA; TRANSCRIPTION FACTORS; VIRULENCE;

MAMMALIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 20044390550     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04479.x     Document Type: Article

References (78)

1. Albus, A.M., Pesci, E.C., Runyen-Janecky, L.J., West, S.E., and Iglewski, B.H. (1997) Vfr controls quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179: 3928-3935.
2. Alm, R.A., and Mattick, J.S. (1995) Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa whose product possesses a prepilin-like leader sequence. Mol Microbiol 16: 485-496.
3. Alm, R.A., and Mattick, J.S. (1996) Identification of two genes with prepilin-like leader sequences required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol 178: 3809-3817.
4. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
5. Andrews, J.M. (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48 (Suppl. 1): 5-16.
6. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S.R., et al. (2002) The Pfam protein families database. Nucleic Acids Res 30: 276-280.
7. Beatson, S.A., Whitchurch, C.B., Sargent, J.L., Levesque, R.C., and Mattick, J.S. (2002a) Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J Bacteriol 184: 3605-3613.
8. Beatson, S.A., Whitchurch, C.B., Semmler, A.B., and Mattick, J.S. (2002b) Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J Bacteriol 184: 3598-3604.
9. Becher, A., and Schweizer, H.P. (2000) Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. Biotechniques 29: 948-950, 952.
10. Bessman, M.J., Frick, D.N., and O'Handley, S.F. (1996) The MutT proteins or 'Nudix' hydrolases, a family of versatile, widely distributed, 'housecleaning' enzymes. J Biol Chem 271: 25059-25062.
11. Bradley, D.E. (1980) A function of Pseudomonas aeruginosa PAO pili: twitching motility. Can J Microbiol 26: 146-154.
12. Bradley, D.E., and Pitt, T.L. (1974) Pilus-dependence of four Pseudomonas aeruginosa bacteriophages with non-contractile tails. J General Virol 23: 1-15.
13. Chi, E., Mehl, T., Nunn, D., and Lory, S. (1991) Interaction of Pseudomonas aeruginosa with A549 pneumocyte cells. Infection Immunity 59: 822-828.
14. Collier, D.N., Anderson, L., McKnight, S.L., Noah, T.L., Knowles, M., Boucher, R., et al. (2002) A bacterial cell to cell signal in the lungs of cystic fibrosis patients. FEMS Microbiol Lett 215: 41-46.
15. Comolli, J., Waite, L., Mostov, K., and Engel, J.N. (1999a) The interaction of Pseudomonas aeruginosa pili and asialo-GM1 stimulates epithelial cell cytotoxicity and bacterial internalization. Infect Immun 67: 3207-3214.
16. Comolli, J.C., Hauser, A.R., Waite, L., Whitchurch, C.B., Mattick, J.S., and Engel, J.N. (1999b) Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia. Infect Immun 67: 3625-3630.
17. D'Argenio, D.A., Calfee, M.W., Rainey, P.B., and Pesci, E.C. (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184: 6481-6489.
18. Dasgupta, N., Ferrell, E.P., Kanack, K.J., West, S.E., and Ramphal, R. (2002) fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is sigma70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J Bacteriol 184: 5240-5250.
19. Deziel, E., Comeau, Y., and Villemur, R. (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183: 1195-1204.
20. Deziel, E., Lepine, F., Milot, S., He, J., Mindrinos, M.N., Tompkins, R.G., and Rahme, L.G. (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2- heptylquinoline in cell-to-cell communication. Proc Natl Acad Sci USA 101: 1339-1344.
21. Diggle, S.P., Winzer, K., Chhabra, S.R., Worrall, K.E., Camara, M., and 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: 29-43.
22. Diggle, S.P., Winzer, K., Lazdunski, A., Williams, P., and Camara, M. (2002) Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J Bacteriol 184: 2576-2586.
23. Doig, P., Todd, T., Sastry, P.A., Lee, K.K., Hodges, R.S., Paranchych, W., and Irvin, R.T. (1988) Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infection Immunity 56: 1641-1646.
24. Engel, J.N. (2003) Molecular pathogenesis of acute Pseudomonas aeruginosa infections. In Severe Infections Caused by Pseudomonas Aeruginosa. Rello, J. (ed). New York: Kluwer Academic/Plenum Press, pp. 201-230.
25. Gallagher, L.A., McKnight, S.L., Kuznetsova, M.S., Pesci, E.C., and Manoil, C. (2002) Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 184: 6472-6480.
26. Giamarellou, H. (2000) Therapeutic guidelines for Pseudomonas aeruginosa infections. Int J Antimicrob Agents 16: 103-106.
27. Guina, T., Purvine, S.O., Yi, E.C., Eng, J., Goodlett, D.R., Aebersold, R., and Miller, S.I. (2003) Quantitative proteomic analysis indicates increased synthesis of a quinolone by Pseudomonas aeruginosa isolates from cystic fibrosis airways. Proc Natl Acad Sci USA 100: 2771-2776.
28. Hahn, H.P. (1997) The type-4 pilus is the major virulence-associated adhesin of Pseudomonas aeruginosa - a review. Gene 192: 99-108.
29. Hauser, A.R., and Engel, J. N. (1999) Pseudomonas aeruginosa includes type-III-secretion-mediated apoptosis of macrophages and epithelial cells. Infect Immun 67: 5530-5537.
30. Hauser, A.R., Kang, P.J., Fleiszig, S.J.M., Mostov, K., and Engel, J. (1998) Defects in type III secretion correlate with internalization of Pseudomonas aeruginosa by epithelial cells. Infect Immun 66: 1413-1420.
31. Henrichsen, J. (1975) The occurrence of twitching motility among Gram-negative bacteria. Acta Path Microbiol Scand Sect B S3: 171-178.
32. Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersboll, B.K., and Molin, S. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146: 2395-2407.
33. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
34. Hoang, T.T., Kutchma, A.J., Becher, A., and Schweizer, H.P. (2000) Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72.
35. Holloway, B.W., and Morgan, A.F. (1986) Genome organisation in Pseudomonas. Annu Rev Microbiol 40: 79-105.
36. Jander, G., Rahme, L.G., and Ausubel, F.M. (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182: 3843-3845.
37. Johnson, K., Parker, M.L., and Lory, S. (1986) Nucleotide sequence and transcriptional initiation site of two Pseudomonas aeruginosa pilin genes. J Biol Chem 261: 15703-15708.
38. Kang, P.J., Hauser, A.R., Apodaca, G., Fleiszig, S.M., Wiener-Kronish, J., Mostov, K., and Engel, J.N. (1997) Identification of Pseudomonas aeruginosa genes required for epithelial cell injury. Mol Microbiol 24: 1249-1262.
39. Klausen, M., Aaes-Jorgensen, A., Molin, S., and Tolker-Nielsen, T. (2003a) Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol 50: 61-68.
40. Klausen, M., Heydorn, A., Ragas, P., Lambertsen, L., Aaes-Jorgensen, A., Molin, S., and Tolker-Nielsen, T. (2003b) Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48: 1511-1524.
41. Kohler, T., Curty, L.K., Barja, F., van Delden, C., and Pechere, J.C. (2000) Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J Bacteriol 182: 5990-5996.
42. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
43. Letunic, I., Goodstadt, L., Dickens, N.J., Doerks, T., Schultz, J., Mott, R., et al. (2002) Recent improvements to the SMART domain-based sequence annotation resource. Nucleic Acids Res 30: 242-244.
44. Liu, P.V. (1966) The roles of various fractions of Pseudomonas aeruginosa in its pathogenesis: identity of the lethal toxins produced in vitro and in vivo. J Infect Dis 116: 481-489.
45. de Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172: 6568-6572.
46. Mattick, J.S. (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56: 289-314.
47. Mattick, J.S., Bills, M.M., Anderson, B.J., Dalrymple, B., Mott, M.R., and Egerton, J.R. (1987) Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J Bacteriol 169: 33-41.
48. Merz, A.J., So, M., and Sheetz, M.P. (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98-102.
49. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
50. Montie, T.C., Craven, R.C., and Holder, I.A. (1982) Flagellar preparations from Pseudomonas aeruginosa: isolation and characterization. Infect Immun 35: 281-288.
51. Morales, V.M., Backman, A., and Bagdasarian, M. (1991) A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants. Gene 97: 39-47.
52. O'Toole, G.A., and Kolter, R. (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30: 295-304.
53. Oliver, A., Canton, R., Campo, P., Baquero, F., and Blazquez, J. (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1254.
54. Rahme, L.G., Ausubel, F.M., Cao, H., Drenkard, E., Goumnerov, B.C., Lau, G.W., et al. (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci USA 97: 8815-8821.
55. Rashid, M.H., and Kornberg, A. (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97: 4885-4890.
56. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbour, NY: Cold Spring Harbor Laboratory Press.
57. Sastry, P.A., Finlay, B.B., Pasloske, B.L., Paranchych, W., Pearlstone, J.R., and Smillie, L.B. (1985) Comparative studies of the amino acid and nucleotide sequences of pilin derived from Pseudomonas aeruginosa PAK and PAO. J Bacteriol 164: 571-577.
58. Schultz, J., Copley, R.R., Doerks, T., Ponting, C.P., and Bork, P. (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28: 231-234.
59. Schultz, J., Milpetz, F., Bork, P., and Ponting, C.P. (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95: 5857-5864.
60. Schweizer, H.P. (1992) Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol Microbiol 6: 1195-1204.
61. Schweizer, H.P., and Hoang, T.T. (1995) An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
62. Semmler, A.B.T., Whitchuch, C.B., and Mattick, J.S. (1999) A re-examination of twitching motility in Pseudomonas aeruginosa. Microbiology 145: 2863-2873.
63. Shen, Y., Chern, M., Silva, F.G., and Ronald, P. (2001) Isolation of a Xanthomonas oryzae pv. oryzae flagellar operon region and molecular characterization of flhF. Mol Plant Microbe Interact 14: 204-213.
64. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/technology 1: 784-791.
65. Skerker, J.M., and Berg, H.C. (2001) Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA 98: 6901-6904.
66. 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 PAO1, an opportunistic pathogen. Nature 406: 959-964.
67. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
68. Tan, M.W., and Ausubel, F.M. (2000) Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3: 29-34.
69. Towbin, H., Staehelin, T., and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76: 4350-4354.
70. Vieira, J., and Messing, J. (1991) New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100: 189-194.
71. Vogel, H.J., and Bonner, D.M. (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem 218: 97-106.
72. Warner, P.T.J.C.P. (1950) The iridescent phenomenon of PS. PYOCYANEA. Brit J Exp Path 31: 242-257.
73. Watson, A.A., Alm, R.A., and Mattick, J.S. (1996) Construction of improved vectors for protein production in Pseudomonas aeruginosa. Gene 172: 163-164.
74. West, S.E., Sample, A.K., and Runyen-Janecky, L.J. (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.
75. Whitchurch, C.B., Leech, A.J., Young, M.D., Kennedy, D.H., Sargent, J.L., Bertrand, J.J., et al. (2004) Characterization of a complex chemosensory signal transduction system which controls twitching motility in Pseudomonas aeruginosa. Mol Microbiol, 52: 873-893.
76. Wolfgang, M.C., Lee, V.T., Gilmore, M.E., and Lory, S. (2003) Coordinate regulation of bacterial virulence genes by a novel adenylate cyclase-dependent signaling pathway. Dev Cell 4: 253-263.
77. Woods, D.E., Straus, D.C., Johanson, W.G., Jr, Berry, V.K., and Bass, J.A. (1980) Role of pili in adherence of Pseudomonas aeruginosa to mammalian buccal epithelial cells. Infection Immunity 29: 1146-1151.
78. Zierdt, C.H. (1971) Autolytic nature of iridescent lysis in Pseudomonas aeruginosa. Antonie Van Leeuwenhoek 37: 319-337.