Lipotoxin F of Pseudomonas aeruginosa is an AlgU-dependent and alginate-independent outer membrane protein involved in resistance to oxidative stress and adhesion to A549 human lung epithelia

Microbiology

Volumn 155, Issue 4, 2009, Pages 1028-1038

  Damro, F Heath ^a   Napper, Jennifer ^a   Teter, M Allison ^b   Yu, Hongwei D ^a,c  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEST VIRGINIA WESLEYAN COLLEGE   (United States)

^c Dow Technology Park   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; BACTERIAL TOXIN; HYDROGEN PEROXIDE; HYPOCHLORITE; LIPOTOXIN F; OUTER MEMBRANE PROTEIN A; UNCLASSIFIED DRUG; ALGU PROTEIN, PSEUDOMONAS AERUGINOSA; BACTERIAL PROTEIN; GLUCURONIC ACID; HEXURONIC ACID; OUTER MEMBRANE PROTEIN; SIGMA FACTOR;

ARTICLE; BACTERIAL SURVIVAL; BACTERIUM ADHERENCE; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE DELETION; LUNG ALVEOLUS EPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; UPREGULATION; CELL LINE; CYTOLOGY; EPITHELIUM CELL; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; HUMAN; LUNG; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

PSEUDOMONAS AERUGINOSA;

ALGINATES; BACTERIAL ADHESION; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL LINE; EPITHELIAL CELLS; GLUCURONIC ACID; HEAT-SHOCK RESPONSE; HEXURONIC ACIDS; HUMANS; LUNG; OXIDATIVE STRESS; PSEUDOMONAS AERUGINOSA; SIGMA FACTOR;

EID: 65649128577     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.025833-0     Document Type: Article

References (49)

1. Babu, M. M., Priya, M. L., Selvan, A. T., Madera, M., Gough, J., Aravind, L. & Sankaran, K. (2006). A database of bacterial lipoproteins (DOLOP) with functional assignments to predicted lipoproteins. J Bacteriol 188, 2761-2773.
2. Baynham, P. J., Ramsey, D. M., Gvozdyev, B. V., Cordonnier, E. M. & Wozniak, D. J. (2006). The Pseudomonas aeruginosa ribbon-helix-helix DNA-binding protein AlgZ (AmrZ) controls twitching motility and biogenesis of type IV pili. J Bacteriol 188, 132-140.
3. Burns, J. L., Gibson, R. L., McNamara, S., Yim, D., Emerson, J., Rosenfeld, M., Hiatt, P., McCoy, K., Castile, R. & other authors (2001). Longitudinal assessment of Pseudomonas aeruginosa in young children with cystic fibrosis. J Infect Dis 183, 444-452.
4. Costerton, J. W. (2001). Cystic fibrosis pathogenesis and the role of biofilms in persistent infection. Trends Microbiol 9, 50-52.
5. Damron, F. H., Qiu, D. & Yu, H. (2009). Pseudomonas aeruginosa sensor kinase KinB negatively controls alginate production through AlgW-dependent MucA proteolysis. J Bacteriol (in press) doi:10.1128/JB.01490-08
6. Davies, D. G., Parsek, M. R., Pearson, J. P., Iglewski, B. H., Costerton, J. W. & Greenberg, E. P. (1998). The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280, 295-298.
7. Deretic, V., Gill, J. F. & Chakrabarty, A. M. (1987). Gene algD coding for GDPmannose dehydrogenase is transcriptionally activated in mucoid Pseudomonas aeruginosa. J Bacteriol 169, 351-358.
8. Feldman, M., Bryan, R., Rajan, S., Scheffler, L., Brunnert, S., Tang, H. & Prince, A. (1998). Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66, 43-51.
9. Figurski, D. H. & Helinski, D. R. (1979). Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648-1652.
10. Firoved, A. M. & Deretic, V. (2003). Microarray analysis of global gene expression in mucoid Pseudomonas aeruginosa. J Bacteriol 185, 1071-1081.
11. E)-dependent promoters (sigmulon) in Pseudofmonas aeruginosa and implications for inflammatory processes in cystic fibrosis. J Bacteriol 184, 1057-1064.
12. Firoved, A. M., Ornatowski, W. & Deretic, V. (2004). Microarray analysis reveals induction of lipoprotein genes in mucoid Pseudomonas aeruginosa: implications for inflammation in cystic fibrosis. Infect Immun 72, 5012-5018.
13. Goldberg, J. B. & Ohman, D. E. (1984). Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate. J Bacteriol 158, 1115-1121.
14. Govan, J. R. & Deretic, V. (1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60, 539-574.
15. Hanna, S. L., Sherman, N. E., Kinter, M. T. & Goldberg, J. B. (2000). Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry. Microbiology 146, 2495-2508.
16. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., Eng, J. K, Akira, S., Underhill, D. M., Aderem, A. & other authors (2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103.
17. Head, N. E. & Yu, H. (2004). Cross-sectional analysis of clinical and environmental isolates of Pseudomonas aeruginosa: biofilm formation, virulence, and genome diversity. Infect Immun 72, 133-144.
18. Hoang, T. T, Kutchma, A. J., Becher, A. & 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.
19. Ishimoto, K S. & Lory, S. (1989). Formation of pilin in Pseudomonas aeruginosa requires the alternative σ factor (RpoN) of RNA polymerase. Proc Natl Acad Sci U S A 86, 1954-1957.
20. Jacob-Dubuisson, F., Locht C. & Antoine, R. (2001). Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol 40, 306-313.
21. Lazar, S. W. & Kolter, R. (1996). SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol 178, 1770-1773.
22. Learn, D. B., Brestel, E P. & Seetharama, S. (1987). Hypochlorite scavenging by Pseudomonas aeruginosa alginate. Infect Immun 55, 1813-1818.
23. Leech, A J., Sprinkle, A., Wood, L, Wozniak D. J. & Ohman, D. E. (2008). The NtrC family regulator AIgB, which controls alginate biosynthesis in mucoid Pseudomonas aeruginosa, binds directly to the algD promoter. J Bacteriol 190, 581-589.
24. Lewenza, S., Gardy, J. L, Brinkman, F. S. & Hancock R. E (2005). Genome-wide identification of Pseudomonas aeruginosa exported proteins using a consensus computational strategy combined with a laboratory-based PhoA fusion screen. Genome Res 15, 321-329.
25. Lyczak, J. B., Cannon, C. L & Pier, G. B. (2002). Lung infections associated with cystic fibrosis. Clin Microbial Rev 15, 194-222.
26. Ma, S., Wozniak D. J. & Ohman, D. E (1997). Identification of the histidine protein kinase KinB in Pseudonumas aeruginosa and its phosphorylation of the alginate regulator algB. J Biol Chem 272, 17952-17960.
27. Ma, S, Selvaraj, U., Ohman, D. E., Quarless, R., Hassett D. J. & WoznlaK D. J. (1998). Phosphorylation-independent activity of the response regulators AIgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa. J Bacteriol 180, 956-968.
28. Martin, D. W., Schurr, M. J., Mudd, M. H., Govan, J. R., Holloway, B. W. & Deretic, V. (1993). Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc Natl Acad Sci U S A 90, 8377-8381.
29. Miller, J. H. (1972). Beta-galactosidase assay. In Exeriments in Molecular Genetics, pp. 352-355. Edited by J. H. Miller. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
30. Nouwens, A. S., Beatson, S. A., Whitchurch, C. B., Walsh, B. J., Schweizer, H. P., Mattick, J. S. & Cordwell, S. J. (2003). Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1. Microbiology 149, 1311-1322.
31. O'Toole, G. A. & Kolter, R. (1998). Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30, 295-304.
32. Oiu, D., Eisinger, V. M., Rowan, D. W. & Yu, H. D. (2007). Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 104, 8107-8112.
33. BAD-based shuttle vectors and functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl Environ Microbiol 74, 7422-7426.
34. Rowen, D. W. & Deretic, V. (2000). Membrane-to-cytosol redistribution of ECF sigma factor AIgU and conversion to mucoidy in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Mol Microbiol 36, 314-327.
35. Salunkhe, P, Smart C. H., Morgan, J. A., Panagea, S., Walshaw, M. J., Hart, C. A., Geffers, R., Tummier, B. & Winstanley, C. (2005). A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. J Bacteriol 187, 4908-4920.
36. E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J Bacteriol 178, 4997-5004.
37. Schuster, M., Lostroh, C. P., Ogi, T. & Greenberg, E. P. (2003). Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185, 2066-2079.
38. Schweizer, H. P. & Hoang, T. T. (1995). An improved system for gene replacement and xyIE fusion analysis in Pseudomonas aeruginosa. Gene 158, 15-22.
39. Singh, P. K., Schaefer, A. L., Parsek, M. R., Moninger, T. O., Welsh, M. J. & Greenberg, E. P. (2000). Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407, 762-764.
40. Skindersoe, M. E., Alhede, M., Phipps, R., Yang, L., Jensen, P. O., Rasmussen, T. B., Bjarnsholt, T., Tolker-Nielsen, T., Høiby, N. & Givskov, M. (2008). Effects of antibiotics on quorum sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 52, 3648-3663.
41. Smith, S. G. J., Mahon, V., Lambert, M. A. & Fagan, R. P. (2007). A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett 273, 1-11.
42. Sriramulu, D. D., Nimtz, M. & Romling, U. (2005). Proteome analysis reveals adaptation of Pseudomonas aeruginosa to the cystic fibrosis lung environment. Proteomics 5, 3712-3721.
43. Tart, A. H., Blanks, M. J. & Wozniak, D. J. (2006). The AlgT-dependent transcriptional regulator AmrZ (AlgZ) inhibits flagellum biosynthesis in mucoid, nonmotile Pseudomonas aeruginosa cystic fibrosis isolates. J Bacteriol 188, 6483-6489.
44. Totten, P. A., Lara, J. C. & Lory, S. (1990). The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J Bacteriol 172, 389-396.
45. 22 (AlgT) and the AlgW and Prc proteases. Mol Microbiol 62, 412-426.
46. Wozniak, D. J. & Keyser, R. (2004). Effects of subinhibitory concentrations of macrolide antibiotics on Pseudomonas aeruginosa. Chest 125, 62S-69S (quiz 69S).
47. Wozniak, D. J. & Ohman, D. E. (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.
48. Zaborina, O., Dhiman, N., Ling Chen, M., Kostal, J., Holder, I. A. & Chakrabarty, A. M. (2000). Secreted products of a nonmucoid Pseudomonas aeruginosa strain induce two modes of macrophage killing: external-ATP-dependent, P2Z-receptor-mediated necrosis and ATP-independent, caspase-mediated apoptosis. Microbiology 146, 2521-2530.
49. Zhang, Z., Louboutin, J. P., Weiner, D. J., Goldberg, J. B. & Wilson, J. M. (2005). Human airway epithelial cells sense Pseudomonas aeruginosa infection via recognition of flagellin by Toll-like receptor 5. Infect Immun 73, 7151-7160.