Long-distance delivery of bacterial virulence factors by pseudomonas aeruginosa outer membrane vesicles

PLoS Pathogens

Volumn 5, Issue 4, 2009, Pages

  Bomberger, Jennifer M ^a   MacEachran, Daniel P ^a   Coutermarsh, Bonita A ^a   Ye, Siying ^a   O'Toole, George A ^a   Stanton, Bruce A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALKALINE PHOSPHATASE; BACTERIAL PROTEIN; BETA LACTAMASE; CYCLE INHIBITING FACTOR; FILIPIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PHOSPHOLIPASE C; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; CELL MEMBRANE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LIPID RAFT; MEMBRANE FUSION; MEMBRANE VESICLE; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PSEUDOMONAS AERUGINOSA; SURFACE PROPERTY; CELL LINE; CONFOCAL MICROSCOPY; CYTOSKELETON; EPITHELIUM CELL; IMMUNOPRECIPITATION; LUNG; METABOLISM; MICROBIOLOGY; MUCOSA; PATHOGENICITY; PHYSIOLOGY; PSEUDOMONAS INFECTION; TRANSPORT VESICLE; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); OAT MOSAIC VIRUS; PSEUDOMONAS AERUGINOSA;

ACTINS; BLOTTING, WESTERN; CELL LINE; CELL MEMBRANE; CYTOSKELETON; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOPRECIPITATION; LUNG; MEMBRANE MICRODOMAINS; MICROSCOPY, CONFOCAL; MUCOUS MEMBRANE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; TRANSPORT VESICLES; VIRULENCE FACTORS; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 66349107694     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000382     Document Type: Article

References (46)

1. Weinstein RA (1998) Nosocomial infection update. Emerg Infect Dis 4: 416-420.
2. Ernst JD (2000) Bacterial Inhibition of Phagocytosis. Cell Microbiol 2: 379-386.
3. Blanke SR (2006) Portals and Pathways: Principles of Bacterial Toxin Entry into Host Cells. Microbe 1: 26-32.
4. Nguyen TT, Saxena A, Beveridge TJ (2003) Effect of surface lipopolysaccharide on the nature of membrane vesicles liberated from the Gram-negative bacterium Pseudomonas aeruginosa. J Electron Microsc (Tokyo) 52: 465-469.
5. Kadurugamuwa JL, Beveridge TJ (1997) Natural release of virulence factors in membrane vesicles by Pseudomonas aeruginosa and the effect of aminoglycoside antibiotics on their release. J Antimicrob Chemother 40: 615-621.
6. Kadurugamuwa JL, Beveridge TJ (1996) Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J Bacteriol 178: 2767-2774.
7. Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177: 3998-4008.
8. Kuehn MJ, Kesty NC (2005) Bacterial outer membrane vesicles and the hostpathogen interaction. Genes Dev 19: 2645-2655.
9. Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437: 422-425.
10. Kato S, Kowashi Y, Demuth DR (2002) Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb Pathog 32: 1-13.
11. Kesty NC, Kuehn MJ (2004) Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J Biol Chem 279: 2069-2076.
12. Wai SN, Lindmark B, Soderblom T, Takade A, Westermark M, et al. (2003) Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115: 25-35.
13. Montes LR, Ibarguren M, Goni FM, Stonehouse M, Vasil ML, et al. (2007) Leakage-free membrane fusion induced by the hydrolytic activity of PlcHR(2), a novel phospholipase C/sphingomyelinase from Pseudomonas aeruginosa. Biochim Biophys Acta 1768: 2365-2372.
14. Bauman SJ, Kuehn MJ (2006) Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect 8: 2400-2408.
15. Kesty NC, Mason KM, Reedy M, Miller SE, Kuehn MJ (2004) Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. Embo J 23: 4538-4549.
16. MacEachran DP, Ye S, Bomberger JM, Hogan DA, Swiatecka-Urban A, et al. (2007) The Pseudomonas aeruginosa secreted protein PA2934 decreases apical membrane expression of the cystic fibrosis transmembrane conductance regulator. Infect Immun 75: 3902-3912.
17. Huang CT, Xu KD, McFeters GA, Stewart PS (1998) Spatial patterns of alkaline phosphatase expression within bacterial colonies and biofilms in response to phosphate starvation. Appl Environ Microbiol 64: 1526-1531.
18. Xu KD, Stewart PS, Xia F, Huang CT, McFeters GA (1998) Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol 64: 4035-4039.
19. Vasil ML, Berka RM, Gray GL, Nakai H (1982) Cloning of a phosphateregulated hemolysin gene (phospholipase C) from Pseudomonas aeruginosa. J Bacteriol 152: 431-440.
20. Vipond C, Wheeler JX, Jones C, Feavers IM, Suker J (2005) Characterization of the protein content of a meningococcal outer membrane vesicle vaccine by polyacrylamide gel electrophoresis and mass spectrometry. Hum Vaccin 1: 80-84.
21. Horstman AL, Kuehn MJ (2000) Enterotoxigenic Escherichia coli secretes active heatlabile enterotoxin via outer membrane vesicles. J Biol Chem 275: 12489-12496.
22. Ye S, Maceachran DP, Hamilton JW, O'Toole GA, Stanton BA (2008) Chemotoxicity of doxorubicin and surface expression of P-glycoprotein (MDR1) is regulated by the Pseudomonas aeruginosa toxin Cif. Am J Physiol Cell Physiol 295: C807-C818.
23. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, et al. (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest 109: 317-325.
24. Harder T, Scheiffele P, Verkade P, Simons K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942.
25. Ellis JA, Luzio JP (1995) Identification and characterization of a novel protein (p137) which transcytoses bidirectionally in Caco-2 cells. J Biol Chem 270: 20717-20723.
26. Caron E, Crepin VF, Simpson N, Knutton S, Garmendia J, et al. (2006) Subversion of actin dynamics by EPEC and EHEC. Curr Opin Microbiol 9: 40-45.
27. McGee K, Zettl M, Way M, Fallman M (2001) A role for N-WASP in invasinpromoted internalisation. FEBS Lett 509: 59-65.
28. Stoorvogel W, Geuze HJ, Griffith JM, Schwartz AL, Strous GJ (1989) Relations between the intracellular pathways of the receptors for transferrin, asialoglycoprotein, and mannose 6-phosphate in human hepatoma cells. J Cell Biol 108: 2137-2148.
29. Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, et al. (1999) Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol 188: 220-226.
30. Lieberman J (2003) The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat Rev Immunol 3: 361-370.
31. Shapiro SD (1994) Elastolytic metalloproteinases produced by human mononuclear phagocytes. Potential roles in destructive lung disease. Am J Respir Crit Care Med 150: S160-S164.
32. Caughey GH (1994) Serine proteinases of mast cell and leukocyte granules. A league of their own. Am J Respir Crit Care Med 150: S138-S142.
33. Azghani AO (1996) Pseudomonas aeruginosa and epithelial permeability: role of virulence factors elastase and exotoxin A. Am J Respir Cell Mol Biol 15: 132-140.
34. Azghani AO, Bedinghaus T, Klein R (2000) Detection of elastase from Pseudomonas aeruginosa in sputum and its potential role in epithelial cell permeability. Lung 178: 181-189.
35. Luberto C, Stonehouse MJ, Collins EA, Marchesini N, El-Bawab S, et al. (2003) Purification, characterization, and identification of a sphingomyelin synthase from Pseudomonas aeruginosa. PlcH is a multifunctional enzyme. J Biol Chem 278: 32733-32743.
36. Stonehouse MJ, Cota-Gomez A, Parker SK, Martin WE, Hankin JA, et al. (2002) A novel class of microbial phosphocholine-specific phospholipases C. Mol Microbiol 46: 661-676.
37. Quakyi EK, Hochstein HD, Tsai CM (1997) Modulation of the biological activities of meningococcal endotoxins by association with outer membrane proteins is not inevitably linked to toxicity. Infect Immun 65: 1972-1979.
38. Schild S, Nelson EJ, Camilli A (2008) Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect Immun 76: 4554-4563.
39. Schorey JS, Bhatnagar S (2008) Exosome function: from tumor immunology to pathogen biology. Traffic 9: 871-881.
40. Bebok Z, Collawn JF, Wakefield J, Parker W, Li Y, et al. (2005) Failure of cAMP agonists to activate rescued deltaF508 CFTR in CFBE41o- airway epithelial monolayers. J Physiol 569: 601-615.
41. Swiatecka-Urban A, Brown A, Moreau-Marquis S, Renuka J, Coutermarsh B, et al. (2005) The short apical membrane half-life of rescued DF508-cystic fibrosis transmembrane conductance regulator (CFTR) results from accelerated endocytosis of DF508-CFTR in polarized human airway epithelial cells. J Biol Chem 280: 36762-36772.
42. Swiatecka-Urban A, Boyd C, Coutermarsh B, Karlson KH, Barnaby R, et al. (2004) Myosin VI regulates endocytosis of the cystic fibrosis transmembrane conductance regulator. J Biol Chem 279: 38025-38031.
43. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, et al. (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci U S A 97: 8815-8821.
44. Butterworth MB, Edinger RS, Ovaa H, Burg D, Johnson JP, et al. (2007) The deubiquitinating enzyme UCH-L3 regulates the apical membrane recycling of the epithelial sodium channel. J Biol Chem 282: 37885-37893.
45. Swiatecka-Urban A, Talebian L, Kanno E, Moreau-Marquis S, Coutermarsh B, et al. (2007) Myosin VB is required for trafficking of CFTR in RAB11A-specific apical recycling endosomes in polarized human airway epithelial cells. J Biol Chem 282: 23725-23736.
46. Pike LJ, Han X, Gross RW (2005) Epidermal growth factor receptors are localized to lipid rafts that contain a balance of inner and outer leaflet lipids: a shotgun lipidomics study. J Biol Chem 280: 26796-26804.