View Item 

Show simple item record

Intracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cells
dc.contributor.authorSajjan, Umadevi S.en_US
dc.contributor.authorYang, Jeffrey H.en_US
dc.contributor.authorHershenson, Marc B.en_US
dc.contributor.authorLiPuma, John J.en_US
dc.date.accessioned2010-06-01T22:46:43Z
dc.date.available2010-06-01T22:46:43Z
dc.date.issued2006-09en_US
dc.identifier.citationSajjan, 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.issn1462-5814en_US
dc.identifier.issn1462-5822en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/75744
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=16922864&dopt=citationen_US
dc.description.abstractWe 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.extent870820 bytes
dc.format.extent3109 bytes
dc.format.mimetypeapplication/pdf
dc.format.mimetypetext/plain
dc.publisherBlackwell Publishing Ltden_US
dc.rights© 2006 The Authors; Journal compilation © 2006 Blackwell Publishing Ltden_US
dc.titleIntracellular trafficking and replication of Burkholderia cenocepacia in human cystic fibrosis airway epithelial cellsen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biologyen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.identifier.pmid16922864en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/75744/1/j.1462-5822.2006.00724.x.pdf
dc.identifier.doi10.1111/j.1462-5822.2006.00724.xen_US
dc.identifier.sourceCellular Microbiologyen_US
dc.identifier.citedreferenceAgodi, 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.citedreferenceAlonso, A., and Garcia-del Protillo, E. ( 2004 ) Hijacking of eukaryotic functions by intracellular bacterial pathogens. Int Microbiol 7: 181 – 191.en_US
dc.identifier.citedreferenceBlommaart, 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.citedreferenceBurns, 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.citedreferenceChen, 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.citedreferenceChiu, 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.citedreferenceChung, 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.citedreferenceComerci, 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.citedreferenceCoyene, 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.citedreferenceDelrue, 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.citedreferenceDuclos, 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.citedreferenceEngledow, 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.citedreferenceGovan, 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.citedreferenceHowe, 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.citedreferenceIsles, 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.citedreferenceJohnson, 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.citedreferenceLamothe, 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.citedreferenceLefebre, 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.citedreferenceLiou, 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.citedreferenceLiPuma, J. J. ( 1998 ) Burkholderia cepacia: management issues and new insights. Clin Chest Med 19: 473 – 486.en_US
dc.identifier.citedreferenceLiPuma, 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.citedreferenceMcKevitt, 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.citedreferenceMahenthiralingam, 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.citedreferenceMahenthiralingam, 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.citedreferenceMartin, D. W., and Mohr, C. D. ( 2000 ) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68: 24 – 29.en_US
dc.identifier.citedreferenceMeijer, 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.citedreferenceMolofsky, 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.citedreferencePitt, 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.citedreferencePizarro-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.citedreferencePizarro-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.citedreferenceReik, 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.citedreferenceSaini, 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.citedreferenceSajjan, 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.citedreferenceSajjan, 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.citedreferenceSajjan, 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.citedreferenceSajjan, 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.citedreferenceSajjan, 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.citedreferenceSchwab, 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.citedreferenceShaw, 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.citedreferenceSokol, 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.citedreferenceSpeert, 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.citedreferenceTomich, 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.citedreferenceTomich, 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.citedreferenceUrban, 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.citedreferenceUrban, 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.citedreferenceValvano, 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.citedreferenceVandamme, 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.citedreferenceVisser, 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.citedreferenceZeitlin, 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.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
j.1462-5822.2006.00724.x.pdf
Size:
850.4KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe its collections in a way that respects the people and communities who create, use, and are represented in them. We encourage you to Contact Us anonymously if you encounter harmful or problematic language in catalog records or finding aids. More information about our policies and practices is available 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.