Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells

Cellular Microbiology

Volumn 8, Issue 9, 2006, Pages 1456-1466

  Sajjan, Umadevi S ^a   Yang, Jeffrey H ^a   Hershenson, Marc B ^a   LiPuma, John J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CALNEXIN; CATHEPSIN D; DANSYLCADAVERINE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; RAB7 PROTEIN;

ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM COLONY; BACTERIUM ISOLATION; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA COMPLEX; CELL CULTURE; CELL VACUOLE; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOPLASM; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM;

ACRIDINE ORANGE; ACTINS; BURKHOLDERIA CEPACIA; CELL LINE, TRANSFORMED; CYSTIC FIBROSIS; CYTOCHALASIN D; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; EPITHELIAL CELLS; HEAT; HUMANS; LYSOSOMES; MICROSCOPY, FLUORESCENCE; RESPIRATORY SYSTEM;

BACTERIA (MICROORGANISMS); BURKHOLDERIA CENOCEPACIA;

EID: 33746891552     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00724.x     Document Type: Article

References (49)

1. Agodi, A., Mahenthiralingam, E., Bachitta, M., Giannino, V., Sciacca, A., and Stefani, S. (2001) Burkholderia cepacia complex infection in Italian patients with cystic fibrosis: Prevalence, epidemiology, and genomovar status. J Clin Microbiol 39: 2891-2896.
2. Alonso, A., and Garcia-del Protillo, E. (2004) Hijacking of eukaryotic functions by intracellular bacterial pathogens. Int Microbiol 7: 181-191.
3. Blommaart, E. F., Krause, U., Schellens, J. P., Vreeling-Sindelarova, H., and Meijer, A. J. (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243: 240-246.
4. Burns, J. L., Jonas, M., Chi, E. Y., Clark, D. K., Berger, A., and Griffith, A. (1996) Invasion of respiratory epithelial cells by Burkholderia (Pseudomonas) cepacia. Infect Immun 64: 4054-4059.
5. Chen, J. S., Witzmann, K. A., Spilker, T., Fink, R. J., and LiPuma, J. J. (2001) Endemicity and inter-city spread of Burkholderia cepacia genomovar III in cystic fibrosis. J Pediatr 139: 643-649.
6. Chiu, C. H., Ostry, A., and Speert, D. P. (2001) Invasion of murine respiratory epithelial cells in vivo by Burkholderia cepacia. J Med Microbiol 50: 594-601.
7. Chung, J. W., Altman, E., Beveridge, T. J., and Speert, D. P. (2003) Colonial morphology of Burkholderia cepacia complex genomovar III: implications in exopolysaccharide production, pilus expression, and persistence in the mouse. Infect Immun 71: 904-909.
8. Comerci, D. J., Martinez-Lorenzo, M. J., Sieira, R., Gorvel, J. P., and Ugalde, R. A. (2001) Essential role of the VirB machinery in the maturation of the Brucella abortus -containing vacuole. Cell Microbiol 3: 159-168.
9. Coyene, T., Vandamme, P., Govan, J. R. W., and LiPuma, J. J. (2001) Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39: 3427-3436.
10. Delrue, R. M., Martinez-Lorenzo, M., Lestrate, P., Danese, I., Bielarz, V., Mertens, P., et al. (2001) Identification of Brucella spp. genes involved in intracellular trafficking. Cell Microbiol 3: 487-497.
11. Duclos, S., and Desjardins, M. (2000) Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2: 365-377.
12. Engledow, A. S., Medrano, E. G., Mahenthiralingam, E., LiPuma, J. J., and Gonzalez, C. F. (2004) Involvement of a plasmid-encoded type IV secretion system in the plant tissue watersoaking phenotype of Burkholderia cenocepacia. J Bacteriol 186: 6015-6024.
13. Govan, J. R. W., and Deretic, V. (1996) Microbial pathogenesis in cystic fibrosis: Mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60: 539-574.
14. Howe, D., Barrows, L. F., Lindstrom, N. M., and Heinzen, R. A. (2002) Nitric oxide inhibits Coxiella burnetti replication and parasitophorous vacuole maturation. Infect Immun 70: 5140-5147.
15. Isles, A., Maclusky, I., Corey, M., Gold, R., Prober, C., Flemming, P., and Levison, H. (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104: 206-210.
16. Johnson, W. M., Tyler, S. D., and Rozee, K. R. (1994) Linkage analysis of geographical and clinical clusters of Pseudomonas cepacia infections by multilocus enzyme electrophoresis and ribotyping. J Clin Microbiol 32: 924-930.
17. Lamothe, J., Thyssen, S., and Valvano, M. A. (2004) Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell Microbiol 6: 1127-1138.
18. Lefebre, M., and Valvano, M. (2001) In vitro resistance of Burkholderia cepacia complex isolates to reactive oxygen species in relation to catalase and superoxide dismutase production. Microbiology 147: 97-109.
19. Liou, T. G., Adler, F. R., Fitzsimmons, S. C., Cahill, B. C., Hibbs, J. R., and Marshall, B. C. (2001) Predictive 5-year survivorship model of cystic fibrosis. Am J Epidemiol 153: 345-352.
20. LiPuma, J. J. (1998) Burkholderia cepacia: Management issues and new insights. Clin Chest Med 19: 473-486.
21. LiPuma, J. J., Spilker, T., Gill, L. H., Campbell, P. W. I., Liu, L., and Mahenthiralingam, E. (2001) Disproportionate distribution of Burkholderia cepacia complex species and transmissibility factors in cystic fibrosis. Am J Respir Crit Care Med 164: 92-96.
22. McKevitt, A. I., Bajaksourzian, S., Klinger, J. D., and Woods, D. E. (1989) Purification and characterization of an extracellular proteases from Psuedomonas cepacia. Infect Immun 57: 771-778.
23. Mahenthiralingam, E., Baldwin, A., and Vandamme, P. (2002) Burkholderia cepacia complex infection in patients with cystic fibrosis. J Med Microbiol 51: 533-538.
24. Mahenthiralingam, E., Urban, T. A., and Goldberg, J. B. (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144-156.
25. Martin, D. W., and Mohr, C. D. (2000) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68: 24-29.
26. Meijer, A. J., and Codogno, P. (2004) Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol 36: 2445-2462.
27. Molofsky, A. B., and Swanson, M. S. (2004) Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29-40.
28. Pitt, T. L., Kaufmann, M. E., Patel, P. S., Benge, L. C., Gaskin, S., and Livermore, D. M. (1996) Type characterisation and antibiotic susceptibility of Burkholderia (Pseudomonas) cepacia isolates from patients with cystic fibrosis in the United Kingdom and the Republic of Ireland. J Med Microbiol 44: 203-210.
29. Pizarro-Cerda, J., Moreno, E., Sanguedolce, V., Mege, J. L., and Gorvel, J. P. (1998) Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387-2392.
30. Pizarro-Cerda, J., Moreno, E., and Gorvel, J. P. (2000) Invasion and intracellular trafficking of Brucella abortus in nonphagocytic cells. Microbes Infect 2: 829-835.
31. Reik, R., Spilker, T., and LiPuma, J. J. (2005) Distribution of Burkholderia cepacia complex species among isolates recovered from persons with or without cystic fibrosis. J Clin Microbiol 43: 2926-2928.
32. Saini, L. S., Galsworthy, S. B., John, M. A., and Valvano, M. A. (1999) Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145: 3465-3475.
33. Sajjan, U., Wu, Y., Kent, G., and Forstner, J. (2000) Preferential adherence of cable-piliated Burkholderia cepacia to respiratory epithelia of CF knockout mice and human cystic fibrosis lung explants. J Med Microbiol 49: 875-885.
34. Sajjan, U., Corey, M., Humar, A., Tullis, E., Cutz, E., Ackerley, C., and Forstner, J. (2001a) Immunolocalization of Burkholderia cepacia in the lungs of cystic fibrosis patients. J Med Microbiol 50: 535-546.
35. Sajjan, U., Thanassoulis, G., Cherapanov, V., Lu, A., Sjolin, C., Steer, B., et al. (2001b) Susceptibility of Cftr (-/-) mice to pulmonary infection with Burkholderia cepacia. Infect Immun 69: 5138-5150.
36. Sajjan, U., Ackerley, C., and Forstner, J. (2002) Interaction of cblA/ Adhesin-positive Burkholderia cepacia with squamous epithelium. Cell Microbiol 4: 73-86.
37. Sajjan, S., Keshavjee, S., and Forstner, J. (2004) Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection. Infect Immun 72: 4188-4199.
38. Schwab, U., Leigh, M., Ribeiro, C., Yankaskas, J., Burns, K., Gilligan, P., et al. (2002) Patterns of epithelial cell invasion by different species of Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect Immun 70: 4547-4555.
39. Shaw, D., Poxton, I. R., and Govan, J. R. (1995) Biological activity of Burkholderia (Pseudomonas) cepacia lipopolysaccharide. FEMS Immunol Med Microbiol 11: 99-106.
40. Sokol, P. A., Sajjan, U., Visser, M. B., Gingues, S., Forstner, J., and Kooi, C. (2003) The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149: 3649-3658.
41. Speert, D., Henry, P., Vandamme, P., Corey, M., and Mahenthiralingam, E. (2002) Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis. Can Emerg Infect Dis 8: 181-187.
42. Tomich, M., Herfst, C. A., Golden, J. W., and Mohr, C. D. (2002) Role of flagella in host cell invasion by Burkholderia cepacia. Infect Immun 70: 1799-1806.
43. Tomich, M., Griffith, A., Herfst, C. A., Burns, J. L., and Mohr, C. D. (2003) Attenuated virulence of a Burkholderia cepacia type III secretion mutant in a murine model of infection. Infect Immun 71: 1405-1415.
44. Urban, T. A., Griffith, A., Torok, A. M., Smolkin, M. E., Burns, J. L., and Goldberg, J. B. (2004) Contribution of Burkholderia cenocepacia flagella to infectivity and inflammation. Infect Immun 72: 5126-5134.
45. Urban, T. A., Goldberg, J. B., Forstner, J. F., and Sajjan, U. S. (2005) Cable pili and the 22-kilodalton adhesin are required for Burkholderia cenocepacia binding to and transmigration across the squamous epithelium. Infect Immun 73: 5426-5437.
46. Valvano, M. A., Keith, K. E., and Cardona, S. T. (2005) Survival and persistence of opportunistic Burkholderia species in host cells. Curr Opin Microbiol 8: 99-105.
47. Vandamme, P., Holmes, B., Coeyne, T., Goris, J., Mahenthiralingam, E., LiPuma, J. J., and Govan, J. R. (2003) Burkholderia cenocepacia sp. nov.-a new twist to an old story. Res Microbiol 154: 91-96.
48. Visser, M. B., Majumdar, S., Hani, E., and Sokol, P. A. (2004) Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections. Infect Immun 72: 2850-2857.
49. Zeitlin, P. L., Lu, L., Rhim, J., Cutting, G., Stetten, G., Kieffer, K. A., et al. (1991) A cystic fibrosis bronchial epithelial cell line: immortalization by adeno-12-SV40 infection. Am J Respir Cell Mol Biol 4: 313-319.