1887

Abstract

is a facultative intracellular pathogen that survives and replicates in phagocytic cell lines. The bacterial burden recovered from naïve BALB/c mice infected by intranasal delivery indicated that persists in the lower respiratory system. To address whether invades respiratory non-professional phagocytes, this study utilized A549 and LA-4 respiratory epithelial cells and demonstrated that possesses the capacity to adhere poorly to, but not to invade, these cells. Furthermore, it was found that was taken up by the murine alveolar macrophage cell line MH-S following serum coating, an attribute suggestive of complement- or Fc receptor-mediated uptake. Invasion/intracellular survival assays of -infected MH-S cells demonstrated decreased intracellular survival, whilst a type III secretion system effector mutant strain survived longer than the wild-type. Evaluation of the potential mechanism(s) responsible for efficient clearing of intracellular organisms demonstrated comparable levels of caspase-3 in both the wild-type and mutant with characteristics consistent with apoptosis of infected MH-S cells. Furthermore, challenge of BALB/c mice with the mutant by the intranasal route resulted in increased survival. Overall, these data suggest that induces apoptotic cell death, whilst the BopA effector protein participates in intracellular survival.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.007724-0
2009-05-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jmm/58/5/554.html?itemId=/content/journal/jmm/10.1099/jmm.0.007724-0&mimeType=html&fmt=ahah

References

  1. Ahmed K., Enciso H. D., Masaki H., Tao M., Omori A., Tharavichikul P., Nagatake T. 1999; Attachment of Burkholderia pseudomallei to pharyngeal epithelial cells: a highly pathogenic bacteria with low attachment ability. Am J Trop Med Hyg 60:90–93
    [Google Scholar]
  2. Alekseev V. V., Savchenko S. T., Iakovlev A. T., Rybkin V. S., Kovalenko A. A., Bykova O. I., Metlin V. N. 1994; The early laboratory diagnosis of the pulmonary form of glanders and melioidosis by using rapid methods of immunochemical analysis. Zh Mikrobiol Epidemiol Immunobiol59–63
    [Google Scholar]
  3. Anuntagool N., Aramsri P., Panichakul T., Wuthiekanun V. R., Kinoshita R., White N. J., Sirisinha S. 2000; Antigenic heterogeneity of lipopolysaccharide among Burkholderia pseudomallei clinical isolates. Southeast Asian J Trop Med Public Health 31 (Suppl. 1):146–152
    [Google Scholar]
  4. Brett P. J., DeShazer D., Woods D. E. 1998; Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei -like species. Int J Syst Bacteriol 48:317–320 [CrossRef]
    [Google Scholar]
  5. Brett P. J., Burtnick M. N., Su H., Nair V., Gherardini F. C. 2008; iNOS activity is critical for the clearance of Burkholderia mallei from infected RAW 264.7 murine macrophages. Cell Microbiol 10:487–498
    [Google Scholar]
  6. Brown N. F., Boddey J. A., Flegg C. P., Beacham I. R. 2002; Adherence of Burkholderia pseudomallei cells to cultured human epithelial cell lines is regulated by growth temperature. Infect Immun 70:974–980 [CrossRef]
    [Google Scholar]
  7. Burtnick M. N., Brett P. J., Woods D. E. 2002; Molecular and physical characterization of Burkholderia mallei O antigens. J Bacteriol 184:849–852 [CrossRef]
    [Google Scholar]
  8. Caignard A., Martin M. S., Hammann A., Martin F. 1985; Heterogeneity of the rat macrophage antigenic specificity of resident peritoneal and pleural macrophages. Cell Mol Biol 31:41–47
    [Google Scholar]
  9. Cieri M. V., Mayer-Hamblett N., Griffith A., Burns J. L. 2002; Correlation between an in vitro invasion assay and a murine model of Burkholderia cepacia lung infection. Infect Immun 70:1081–1086 [CrossRef]
    [Google Scholar]
  10. Coenye T., Vandamme P., Govan J. R., LiPuma J. J. 2001; Taxonomy and identification of the Burkholderia cepacia complex. J Clin Microbiol 39:3427–3436 [CrossRef]
    [Google Scholar]
  11. Cullinane M., Gong L., Li X., Lazar-Adler N., Tra T., Wolvetang E., Prescott M., Boyce J. D., Devenish R. J., Adler B. 2008; Stimulation of autophagy suppresses the intracellular survival of Burkholderia pseudomallei in mammalian cell lines. Autophagy 4:744–753 [CrossRef]
    [Google Scholar]
  12. Decker T., Lohmann-Matthes M. L. 1988; A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J Immunol Methods 115:61–69 [CrossRef]
    [Google Scholar]
  13. Ermolaeva M. D., White O., Salzberg S. L. 2001; Prediction of operons in microbial genomes. Nucleic Acids Res 29:1216–1221 [CrossRef]
    [Google Scholar]
  14. Gao L. Y., Kwaik Y. A. 2000; The modulation of host cell apoptosis by intracellular bacterial pathogens. Trends Microbiol 8:306–313 [CrossRef]
    [Google Scholar]
  15. Harmsen A. G., Muggenburg B. A., Snipes M. B., Bice D. E. 1985; The role of macrophages in particle translocation from lungs to lymph nodes. Science 230:1277–1280 [CrossRef]
    [Google Scholar]
  16. Hauser A. R., Engel J. N. 1999; Pseudomonas aeruginosa induces type-III-secretion-mediated apoptosis of macrophages and epithelial cells. Infect Immun 67:5530–5537
    [Google Scholar]
  17. Hersh D., Monack D. M., Smith M. R., Ghori N., Falkow S., Zychlinsky A. 1999; The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci U S A 96:2396–2401 [CrossRef]
    [Google Scholar]
  18. Hilbi H., Moss J. E., Hersh D., Chen Y., Arondel J., Banerjee S., Flavell R. A., Yuan J., Sansonetti P. J., Zychlinsky A. 1998; Shigella -induced apoptosis is dependent on caspase-1 which binds to IpaB. J Biol Chem 273:32895–32900 [CrossRef]
    [Google Scholar]
  19. Isles A., Maclusky I., Corey M., Gold R., Prober C., Fleming P., Levison H. 1984; Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104:206–210 [CrossRef]
    [Google Scholar]
  20. Jennings W. E. 1963; Diseases transmitted from animals to man. In Glanders pp 264–292 Edited by Hull T. G. Springfield, IL: Charles C. Thomas;
    [Google Scholar]
  21. Kespichayawattana W., Rattanachetkul S., Wanun T., Utaisincharoen P., Sirisinha S. 2000; Burkholderia pseudomallei induces cell fusion and actin-associated membrane protrusion: a possible mechanism for cell-to-cell spreading. Infect Immun 68:5377–5384 [CrossRef]
    [Google Scholar]
  22. Kohler H., Rodrigues S. P., McCormick B. A. 2002; Shigella flexneri interactions with the basolateral membrane domain of polarized model intestinal epithelium: role of lipopolysaccharide in cell invasion and in activation of the mitogen-activated protein kinase ERK. Infect Immun 70:1150–1158 [CrossRef]
    [Google Scholar]
  23. Lever M. S., Nelson M., Ireland P. I., Stagg A. J., Beedham R. J., Hall G. A., Knight G., Titball R. W. 2003; Experimental aerogenic Burkholderia mallei (glanders) infection in the BALB/c mouse. J Med Microbiol 52:1109–1115 [CrossRef]
    [Google Scholar]
  24. Mandell G., Bennett J., Dolin R. 1995; Pseudomonas species (including melioidosis and glanders). In Principles and Practices of Infectious Diseases pp 2006–2007 Edited by Mandell G., Bennett J., Dolin R. New York: Churchill Livingstone;
    [Google Scholar]
  25. Monack D., Falkow S. 2000; Apoptosis as a common bacterial virulence strategy. Int J Med Microbiol 290:7–13 [CrossRef]
    [Google Scholar]
  26. Ogawa M., Suzuki T., Tatsuno I., Abe H., Sasakawa C. 2003; IcsB, secreted via the type III secretion system, is chaperoned by IpgA and required at the post-invasion stage of Shigella pathogenicity. Mol Microbiol 48:913–931 [CrossRef]
    [Google Scholar]
  27. Ribot W. J., Ulrich R. L. 2006; The animal pathogen-like type III secretion system is required for the intracellular survival of Burkholderia mallei within J774.2 macrophages. Infect Immun 74:4349–4353 [CrossRef]
    [Google Scholar]
  28. Rotz L. D., Khan A. S., Lillibridge S. R., Ostroff S. M., Hughes J. M. 2002; Public health assessment of potential biological terrorism agents. Emerg Infect Dis 8:225–230 [CrossRef]
    [Google Scholar]
  29. Srinivasan A., Kraus C. N., DeShazer D., Becker P. M., Dick J. D., Spacek L., Bartlett J. G., Byrne W. R., Thomas D. L. 2001; Glanders in a military research microbiologist. N Engl J Med 345:256–258 [CrossRef]
    [Google Scholar]
  30. Stevens M. P., Haque A., Atkins T., Hill J., Wood M. W., Easton A., Nelson M., Underwood-Fowler C., Titball R. W. other authors 2004; Attenuated virulence and protective efficacy of a Burkholderia pseudomallei bsa type III secretion mutant in murine models of melioidosis. Microbiology 150:2669–2676 [CrossRef]
    [Google Scholar]
  31. Stevens J. M., Ulrich R. L., Taylor L. A., Wood M. W., Deshazer D., Stevens M. P., Galyov E. E. 2005; Actin-binding proteins from Burkholderia mallei and Burkholderia thailandensis can functionally compensate for the actin-based motility defect of a Burkholderia pseudomallei bimA mutant. J Bacteriol 187:7857–7862 [CrossRef]
    [Google Scholar]
  32. Sun G. W., Lu J., Pervaiz S., Cao W. P., Gan Y. H. 2005; Caspase-1 dependent macrophage death induced by Burkholderia pseudomallei . Cell Microbiol 7:1447–1458 [CrossRef]
    [Google Scholar]
  33. Suparak S., Kespichayawattana W., Haque A., Easton A., Damnin S., Lertmemongkolchai G., Bancroft G. J., Korbsrisate S. 2005; Multinucleated giant cell formation and apoptosis in infected host cells is mediated by Burkholderia pseudomallei type III secretion protein BipB. J Bacteriol 187:6556–6560 [CrossRef]
    [Google Scholar]
  34. Ulrich R. L., DeShazer D. 2004; Type III secretion: a virulence factor delivery system essential for the pathogenicity of Burkholderia mallei . Infect Immun 72:1150–1154 [CrossRef]
    [Google Scholar]
  35. Utaisincharoen P., Tangthawornchaikul N., Kespichayawattana W., Anuntagool N., Chaisuriya P., Sirisinha S. 2000; Kinetic studies of the production of nitric oxide (NO) and tumour necrosis factor-alpha (TNF- α ) in macrophages stimulated with Burkholderia pseudomallei endotoxin. Clin Exp Immunol 122:324–329 [CrossRef]
    [Google Scholar]
  36. Waterman S. R., Holden D. W. 2003; Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 5:501–511 [CrossRef]
    [Google Scholar]
  37. Weinrauch Y., Zychlinsky A. 1999; The induction of apoptosis by bacterial pathogens. Annu Rev Microbiol 53:155–187 [CrossRef]
    [Google Scholar]
  38. White N. J. 2003; Melioidosis. Lancet 361:1715–1722 [CrossRef]
    [Google Scholar]
  39. Whitlock G. C., Estes D. M., Torres A. G. 2007; Glanders: off to the races with Burkholderia mallei . FEMS Microbiol Lett 277:115–122 [CrossRef]
    [Google Scholar]
  40. Whitlock G. C., Estes D. M., Young G., Young B., Torres A. G. 2008; Construction of a reporter system to study Burkholderia mallei type III secretion and identification of the BopA effector protein function in intracellular survival. Trans R Soc Trop Med Hyg 102 (Suppl. 1):S127–S133 [CrossRef]
    [Google Scholar]
  41. Wiersinga W. J., de Vos A. F., de Beer R., Wieland C. W., Roelofs J. J., Woods D. E., van der Poll T. 2008; Inflammation patterns induced by different Burkholderia species in mice. Cell Microbiol 10:81–87
    [Google Scholar]
  42. Yan L., Cirillo J. D. 2004; Infection of murine macrophage cell lines by Legionella pneumophila . FEMS Microbiol Lett 230:147–152 [CrossRef]
    [Google Scholar]
  43. Zhou D., Galan J. 2001; Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect 3:1293–1298 [CrossRef]
    [Google Scholar]
  44. Zychlinsky A., Prevost M. C., Sansonetti P. J. 1992; Shigella flexneri induces apoptosis in infected macrophages. Nature 358:167–169 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.007724-0
Loading
/content/journal/jmm/10.1099/jmm.0.007724-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error