Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells
dc.contributor.author | Sajjan, Umadevi S. | en_US |
dc.contributor.author | Yang, Jeffrey H. | en_US |
dc.contributor.author | Hershenson, Marc B. | en_US |
dc.contributor.author | LiPuma, John J. | en_US |
dc.date.accessioned | 2010-06-01T22:46:43Z | |
dc.date.available | 2010-06-01T22:46:43Z | |
dc.date.issued | 2006-09 | en_US |
dc.identifier.citation | Sajjan, Umadevi S.; Yang, Jeffrey H.; Hershenson, Marc B.; LiPuma, John J. (2006). "Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells." Cellular Microbiology 8(9): 1456-1466. <http://hdl.handle.net/2027.42/75744> | en_US |
dc.identifier.issn | 1462-5814 | en_US |
dc.identifier.issn | 1462-5822 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/75744 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=16922864&dopt=citation | en_US |
dc.description.abstract | We investigated the trafficking of Burkholderia cenocepacia , an opportunistic respiratory pathogen of persons with cystic fibrosis (CF), in immortalized CF airway epithelial cells in vitro . Our results indicate that bacteria enter cells in a process involving actin rearrangement. Whereas both live and heat-killed bacteria reside transiently in early endosomes, only live bacteria escape from late endosomes to colocalize in vesicles positive for lysosomal membrane marker LAMP1, endoplasmic reticulum (ER) membrane marker calnexin, and autophagosome marker monodansylcadavarine (MDC). Twenty-four hours after infection, microcolonies of live bacteria were observed in the perinuclear area colocalizing with calnexin. In contrast, after ingestion, dead bacteria colocalized with late endosome marker Rab7, and lysosome markers LAMP1 and cathepsin D, but not with calnexin or MDC. Six to eight hours after ingestion of dead bacteria, degraded bacterial particles were observed in the cytoplasm and in vesicles positive for cathepsin D. These results indicate that live B. cenocepacia gain entry into human CF airway cells by endocytosis, escape from late endosomes to enter autophagosomes that fail to fuse with mature lysosomes, and undergo replication in the ER. This survival and replication strategy may contribute to the capacity of B. cenocepacia to persist in the lungs of infected CF patients. | en_US |
dc.format.extent | 870820 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Publishing Ltd | en_US |
dc.rights | © 2006 The Authors; Journal compilation © 2006 Blackwell Publishing Ltd | en_US |
dc.title | Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Molecular, Cellular and Developmental Biology | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.identifier.pmid | 16922864 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/75744/1/j.1462-5822.2006.00724.x.pdf | |
dc.identifier.doi | 10.1111/j.1462-5822.2006.00724.x | en_US |
dc.identifier.source | Cellular Microbiology | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Alonso, A., and Garcia-del Protillo, E. ( 2004 ) Hijacking of eukaryotic functions by intracellular bacterial pathogens. Int Microbiol 7: 181 – 191. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Duclos, S., and Desjardins, M. ( 2000 ) Subversion of a young phagosome: the survival strategies of intracellular pathogens. Cell Microbiol 2: 365 – 377. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Govan, J. R. W., and Deretic, V. ( 1996 ) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60: 539 – 574. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | LiPuma, J. J. ( 1998 ) Burkholderia cepacia: management issues and new insights. Clin Chest Med 19: 473 – 486. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Mahenthiralingam, E., Baldwin, A., and Vandamme, P. ( 2002 ) Burkholderia cepacia complex infection in patients with cystic fibrosis. J Med Microbiol 51: 533 – 538. | en_US |
dc.identifier.citedreference | Mahenthiralingam, E., Urban, T. A., and Goldberg, J. B. ( 2005 ) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3: 144 – 156. | en_US |
dc.identifier.citedreference | Martin, D. W., and Mohr, C. D. ( 2000 ) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68: 24 – 29. | en_US |
dc.identifier.citedreference | Meijer, A. J., and Codogno, P. ( 2004 ) Regulation and role of autophagy in mammalian cells. Int J Biochem Cell Biol 36: 2445 – 2462. | en_US |
dc.identifier.citedreference | Molofsky, A. B., and Swanson, M. S. ( 2004 ) Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29 – 40. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Sajjan, U., Ackerley, C., and Forstner, J. ( 2002 ) Interaction of cblA /Adhesin-positive Burkholderia cepacia with squamous epithelium. Cell Microbiol 4: 73 – 86. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | Shaw, D., Poxton, I. R., and Govan, J. R. ( 1995 ) Biological activity of Burkholderia ( Pseudomonas ) cepacia lipopolysaccharide. FEMS Immunol Med Microbiol 11: 99 – 106. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.identifier.citedreference | 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. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.