Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa

Infection and Immunity

Volumn 74, Issue 6, 2006, Pages 3134-3147

  Zulianello, Laurence ^a   Canard, Coralie ^a   Köhler, Thilo ^a   Caille, Dorothée ^a   Lacroix, Jean Silvain ^b   Meda, Paolo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ELASTASE; LIPOPOLYSACCHARIDE; RHAMNOLIPID; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ADULT; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BASOLATERAL MEMBRANE; CELL INFILTRATION; CELL INVASION; CELL MEMBRANE PERMEABILITY; CELL SECRETION; CHRONIC RESPIRATORY TRACT DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; CYSTIC FIBROSIS; FEMALE; HOST PATHOGEN INTERACTION; HUMAN; HUMAN TISSUE; IMMUNE DEFICIENCY; IN VITRO STUDY; INTERNALIZATION; MALE; NONHUMAN; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; RESPIRATORY EPITHELIUM; TIGHT JUNCTION;

ADULT; CELL SURVIVAL; EPITHELIAL CELLS; FEMALE; GLYCOLIPIDS; HUMANS; MALE; MIDDLE AGED; NASAL MUCOSA; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; VIRULENCE FACTORS;

EID: 33646908499     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01772-05     Document Type: Article

References (59)

1. Avdeef, A. 2001. Physicochemical profiling (solubility, permeability and charge state). Curr. Top. Med. Chem. 1:277-351.
2. Azghani, A. O. 1996. Pseudomonas aeruginosa and epithelial permeability: a role of virulence factors elastase and exotoxin A. Am. J. Respir. Cell Mol. Biol. 15:132-140.
3. Azghani, A. O., T. Bedinghaus, and R. Klein. 2000. Detection of elastase from Pseudomonas aeruginosa in sputum and its potential role in epithelial cell permeability. Lung 178:181-189.
4. Azghani, A. O., J. C. Connelly, B. T. Peterson, L. D. Gray, M. L. Collins, and A. R. Johnson. 1990. Effects of Pseudomonas aeruginosa elastase on alveolar epithelial permeability in guinea pig. Infect. Immun. 58:433-438.
5. Azghani, A. O., L. D. Gray, and A. R. Johnson. 1993. A bacterial protease perturbs the paracellular barrier function of transporting epithelial monolayers in culture. Infect. Immun. 61:2682-2686.
6. Boles, B. R., M. Thoendel, and P. K. Singh. 2005. Rhamnolipids mediate detachment of Pseudomonas aeruginosa from biofilms. Mol. Microbiol. 57: 1210-1223.
7. Cebular, S., S. Lee, P. Tolaney, and L. Lutwick. 2003. Community-acquired pneumonia in immunocompromised patients. Opportunistic infections to consider in differential diagnosis. Postgrad. Med. 113:65-66, 69-70, 73-74.
8. Charollais, A., V. Serre, C. Mock, F. Cogne, D. Bosco, and P. Meda. 1999. Loss of α1 connexin does not alter the prenatal differentiation of pancreatic beta cells and leads to the identification of another islet cell connexin. Dev. Genet. 24:13-26.
9. Coraux, C., C. Kileztky, M. Polette, J. Hinnrasky, J. M. Zahm, P. Devillier, B. S. De, and E. Puchelle. 2004. Airway epithelial integrity is protected by a long-acting β2-adrenergic receptor agonist. Am. J. Respir. Cell Mol. Biol. 30:605-612.
10. Cornelis, G. R., and F. Van Gijsegem. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
11. Cowell, B. A., S. S. Twining, J. A. Hobden, M. S. Kwong, and S. M. Fleiszig. 2003. Mutation of lasA and lasB reduces Pseudomonas aeruginosa invasion of epithelial cells. Microbiology 149:2291-2299.
12. Dacheux, D., I. Attree, and B. Toussaint. 2001. Expression of ExsA in trans confers type III secretion system-dependent cytotoxicity on noncytotoxic Pseudomonas aeruginosa cystic fibrosis isolates. Infect. Immun. 69:538-542.
13. Dacheux, D., B. Toussaint, M. Richard, G. Brochier, J. Croize, and I. Attree. 2000. Pseudomonas aeruginosa cystic fibrosis isolates induce rapid type III secretion-dependent, but exoU-independent, oncosis of macrophages and polymorphonuclear neutrophils. Infect. Immun. 68:2916-2964.
14. Darling, K. E., A. Dewar, and T. J. Evans. 2004. Role of the cystic fibrosis transmembrane conductance regulator in internalization of Pseudomonas aeruginosa by polarized respiratory epithelial cells. Cell. Microbiol. 6:521-533.
15. Davey, M. E., N. C. Caiazza, and G. A. O'Toole. 2003. Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185:1027-1036.
16. de Bentzmann, D., C. Plotkowski, and E. Puchelle. 1996. Receptors in the Pseudomonas aeruginosa adherence to injured and repairing airway epithelium. Am. J. Respir. Crit. Care Med. 154:5155-5162.
17. Espinosa-Urgel, M. 2003. Resident parking only: rhamnolipids maintain fluid channels in biofilms. J. Bacteriol. 185:699-700.
18. Evans, D. J., I. A. Maltseva, J. Wu, and S. M. Fleiszig. 2002. Pseudomonas aeruginosa internalization by corneal epithelial cells involves MEK and ERK signal transduction proteins. FEMS Microbiol. Lett. 213:73-79.
19. Fleiszig, S. M., D. J. Evans, N. Do, V. Vallas, S. Shin, and K. E. Mostov. 1997. Epithelial cell polarity affects susceptibility to Pseudomonas aeruginosa invasion and cytotoxicity. Infect. Immun. 65:2861-2867.
20. Fleiszig, S. M., J. P. Wiener-Kronish, H. Miyazaki, et al. 1997. Pseudomonas aeruginosa-mediated cytotoxicity and invasion correlate with distinct genotypes at the loci encoding exoenzyme S. Infect. Immun. 65:579-586.
21. Garcia-Medina, R., W. M. Dunne, P. K. Singh, and S. L. Brody. 2005. Pseudomonas aeruginosa acquires biofilm-like properties within airway epithelial cells. Infect. Immun. 73:8298-8305.
22. Goldberg, J. B., and G. B. Pier. 2000. The role of CFTR in susceptibility to Pseudomonas aeruginosa infections in cystic fibrosis. Trends Microbiol. 8:514-520.
23. Graham, A., D. M. Steel, R. Wilson, P. J. Cole, E. W. Alton, and D. M. Geddes. 1993. Effects of purified Pseudomonas rhamnolipids on bioelectric properties of sheep tracheal epithelium. Exp. Lung Res. 19:77-89.
24. Hirakata, Y., B. Finlay, D. A. Simpson, S. Kohno, S. Kamihira, and D. P. Speert. 2000. Penetration of clinical isolates of Pseudomonas aeruginosa through MDCK epithelial cell monolayers. J. Infect. Dis. 181:765-769.
25. Hovey, A. K., and D. W. Frank. 1995. Analyses of the DNA-binding and transcriptional activation properties of ExsA, the transcriptional activator of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 177:4427-4436.
26. Immundo, L., J. Barasch, A. Prince, and Q. Al-Awqati. 1995. Cystic fibrosis epithelial cells have a receptor for pathogenic bacteria on their apical surface. Proc. Natl. Acad. Sci. USA 92:3019-3023.
27. Irie, Y., G. A. O'Toole, and M. H. Yuk. 2005. Pseudomonas aeruginosa rhamnolipids disperse Bordetella bronchiseptica biofilms. FEMS Microbiol. Lett. 250:237-243.
28. Kanthakumar, K., G. W. Taylor, D. R. Cundell, R. B. Dowling, M. K. Johnson, P. J. Cole, and R. Wilson. 1996. The effect of bacterial toxin on levels of intracellular adenosine nucleotides and human ciliary beat frequency. Pulm. Pharmacol. 9:223-230.
29. Karp, P. H., T. O. Moninger, S. P. Weber, T. S. Nesselhauf, J. L. Launspach, J. Zabner, and M. J. Welsh. 2002. An in vitro model of differentiated human airway epithelia. Methods for establishing primary cultures. Methods Mol. Biol. 188:115-137.
30. Kazmierczak, B. I., K. Mostov, and J. N. Engel. 2004. Epithelial cell polarity alters Rho-GTPase responses to Pseudomonas aeruginosa. Mol. Biol. Cell 15:411-419.
31. Kierbel, A., A. Gassama-Diagne, K. Mostov, and J. N. Engel. 2005. The phosphoinositol-3-kinase-protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol. Biol. Cell 16:2577-2585.
32. 31a. Kohler, T., L. K. Curty, F. Barja, C. van Delden, and J. C. Pechere. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182:5990-5996.
33. Kowalski, M. P., and G. B. Pier. 2004. Localization of cystic fibrosis transmembrane conductance regulator to lipid rafts of epithelial cells is required for Pseudomonas aeruginosa-induced cellular activation. J. Immunol. 172: 418-425.
34. Kownatzki, R., B. Tummler, and G. Doring. 1987. Rhamnolipid of Pseudomonas aeruginosa in sputum of cystic fibrosis patients. Lancet i:1026-1027.
35. Lee, V. T., R. S. Smith, B. Tummler, and S. Lory. 2005. Activities of Pseudomonas aeruginosa effectors secreted by the type III secretion system in vitro and during infection. Infect. Immun. 73:1695-1705.
36. Maeda, H., and T. Yamamoto. 1996. Pathogenic mechanisms induced by microbial proteases in microbial infections. Biol. Chem. Hoppe-Seyler 377: 217-226.
37. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
38. Matter, K., and M. S. Balda. 2003. Signalling to and from tight junctions. Nat. Rev. Mol. Cell. Biol. 4:225-236.
39. McClure, C. D., and N. L. Schiller. 1996. Inhibition of macrophage phagocytosis by Pseudomonas aeruginosa rhamnolipids in vitro and in vivo. Curr. Microbiol. 33:109-117.
40. McCormick, B. A. 2003. The use of transepithelial models to examine host-pathogen interactions. Curr. Opin. Microbiol. 6:77-81.
41. Morihara, K. 1995. Pseudolysin and other pathogen endopeptidases of thermolysin family. Methods Enzymol. 248:242-253.
42. Moss, J., M. E. Ehrmantraut, B. D. Banwart, D. W. Frank, and J. T. Barieri. 2001. Sera from adult patients with cystic fibrosis contain antibodies to Pseudomonas aeruginosa type III apparatus. Infect. Immun. 69:1185-1188.
43. Pesci, E. C., J. P. Pearson, P. C. Seed, and B. H. Iglewski. 1997. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J. Bacteriol. 179:3127-3132.
44. Pier, G. B. 2002. CFTR mutations and host susceptibility to Pseudomonas aeruginosa lung infection. Curr. Opin. Microbiol. 5:81-86.
45. Plotkowski, M. C., S. Bentzmann, S. H. M. Perieira, J.-M. Zham, O. Bajolet-Laudinat, P. Roger, and E. Puchelle. 1999. Pseudomonas aeruginosa internalization by human epithelial respiratory cells depends on cell differentiation, polarity, and junctional complex integrity. Am. J. Respir. Cell Mol. Biol. 20:880-890.
46. Raymond, D. P., S. J. Pelletier, T. D. Crabtree, H. L. Evans, T. L. Pruett, and R. G. Sawyer. 2003. Impact of antibiotic-resistant Gram-negative bacilli infections on outcome in hospitalized patients. Crit. Care Med. 31:1035-1041.
47. Siegmund, I., and F. Wagner. 1991. New method for detecting rhamnolipids excreted by Pseudomonas species during growth in mineral agar. Biotechnol. Tech. 5:265-268.
48. Singh, P. K., A. L. Schaefer, M. R. Parsek, T. O. Moninger, M. J. Welsh, and E. P. Greenberg. 2000. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762-764.
49. Smith, R. S., and B. H. Iglewski. 2003. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6:56-60.
50. Soell, M., E. Lett, F. Holveck, M. Scholler, D. Wachsmann, and J. P. Klein. 1995. Activation of human monocytes by streptococcal rhamnose glucose polymers is mediated by CD14 antigen, and mannan binding protein inhibits TNF-α release. J. Immunol. 154:851-860.
51. Tillman, T., and M. Cascio. 2003. Effects of membrane lipids on ion channel structure and function. Cell Biochem. Biophys. 38:161-190.
52. Tsukita, S., M. Furuse, and M. Itoh. 2001. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell. Biol. 2:285-293.
53. van Delden, C., and B. H. Iglewski. 1998. Cell to cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 4:551-560.
54. Walters, R. W., P. Freimuth, T. O. Moninger, I. Ganske, J. Zabner, and G. I. Welsh. 2002. Adenovirus fiber disrupts CAR-mediated intercellular adhesion allowing virus escape. Cell 110:789-799.
55. Winzer, K., and P. Williams. 2001. Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. Int. J. Med. Microbiol. 291:131-143.
56. Yamamoto, N., M. W. Petroll, H. D. Cavanagh, and J. V. Jester. 2005. Internalization of Pseudomonas aeruginosa is mediated by lipid rafts in contact lens-wearing rabbit and cultured human corneal epithelial cells. Investig. Ophthalmol. Vis. Sci. 46:1348-1355.
57. Yanagihara, K., K. Tomono, Y. Kaneko, Y. Miyazaki, K. Tsukamoto, Y. Hirakata, H. Mukae, J. Kadota, I. Murata, and S. Kohno. 2003. Role of elastase in a mouse model of chronic respiratory Pseudomonas aeruginosa infection that mimics diffuse panbronchiolitis. J. Med. Microbiol. 52:531-535.
58. Yi, X., Y. Wang, and F. S. Yu. 2000. Corneal epithelial tight junctions and their response to lipopolysaccharide challenge. Investig. Ophthalmol. Vis. Sci. 41:4093-5100.
59. Zulianello, L., K. Kaneko, M. Scott, S. Erpel, D. Han, F. E. Cohen, and S. B. Prusiner. 2000. Dominant-negative inhibition of prion formation diminished by deletion mutagenesis of the prion protein. J. Virol. 74: 4351-4360.