1887

Abstract

is an important human pathogen in patients with cystic fibrosis (CF). Non-clinical reservoirs may play a role in the acquisition of infection, so it is important to evaluate the pathogenic potential of environmental isolates. In this study, we investigated the interactions of two environmental strains (Mex1 and MCII-168) with two bronchial epithelial cell lines, 16HBE14o and CFBE41o, which have a non-CF and a CF phenotype, respectively. The environmental strains showed a significantly lower level of invasion into both CF and non-CF cells in comparison with the clinical LMG16656 strain. Exposure of polarized CFBE41o or 16HBE14o cells to the environmental strains resulted in a significant reduction in transepithelial resistance (TER), comparable with that observed following exposure to the clinical strain. A different mechanism of tight junction disruption in CF versus non-CF epithelia was found. In the 16HBE41o cells, the environmental strains resulted in a drop in TER without any apparent effect on tight junction proteins such as zonula occludens-1 (ZO-1). In contrast, in CF cells, the amount of ZO-1 and its localization were clearly altered by the presence of both the environmental strains, comparable with the effect of LMG16656. This study demonstrates that even if the environmental strains are significantly less invasive than the clinical strain, they have an effect on epithelial integrity comparable with that of the clinical strain. Finally, the tight junction regulatory protein ZO-1 appears to be more susceptible to the presence of environmental strains in CF cells than in cells which express a functional cystic fibrosis transmembrane regulator (CFTR).

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.056986-0
2012-05-01
2020-07-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/5/1325.html?itemId=/content/journal/micro/10.1099/mic.0.056986-0&mimeType=html&fmt=ahah

References

  1. Baldwin A., Sokol P. A., Parkhill J., Mahenthiralingam E.. ( 2004;). The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia . Infect Immun72:1537–1547
    [Google Scholar]
  2. Baldwin A., Mahenthiralingam E., Drevinek P., Vandamme P., Govan J. R. W., Waine D. J., LiPuma J. J., Chiarini L., Dalmastri C.. & other authors ( 2007;). Environmental Burkholderia cepacia complex isolates in human infections. Emerg Infect Dis13:458–461 [CrossRef][PubMed]
    [Google Scholar]
  3. Becker K. A., Riethmüller J., Zhang Y., Gulbins E.. ( 2010;). The role of sphingolipids and ceramide in pulmonary inflammation in cystic fibrosis. Open Respir Med J4:39–47[PubMed]
    [Google Scholar]
  4. Berg G., Eberl L., Hartmann A.. ( 2005;). The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol7:1673–1685 [CrossRef][PubMed]
    [Google Scholar]
  5. Bevivino A., Dalmastri C., Tabacchioni S., Chiarini L., Belli M. L., Piana S., Materazzo A., Vandamme P., Manno G.. ( 2002;). Burkholderia cepacia complex bacteria from clinical and environmental sources in Italy: genomovar status and distribution of traits related to virulence and transmissibility. J Clin Microbiol40:846–851 [CrossRef][PubMed]
    [Google Scholar]
  6. Cao H., Baldini R. L., Rahme L. G.. ( 2001;). Common mechanisms for pathogens of plants and animals. Annu Rev Phytopathol39:259–284 [CrossRef][PubMed]
    [Google Scholar]
  7. Chiarini L., Tabacchioni S., Bevivino A., Dalmastri C., Manno G., Ugolotti E., Piana S.. ( 2002;). B. cepacia genomovar III: is the subdivision in two recA groups related to different degree of virulence?. J Cyst Fibros 1 Suppl. 162
    [Google Scholar]
  8. Chiarini L., Cescutti P., Drigo L., Impallomeni G., Herasimenka Y., Bevivino A., Dalmastri C., Tabacchioni S., Manno G.. & other authors ( 2004;). Exopolysaccharides produced by Burkholderia cenocepacia recA lineages IIIA and IIIB. J Cyst Fibros3:165–172 [CrossRef][PubMed]
    [Google Scholar]
  9. Chiarini L., Bevivino A., Dalmastri C., Tabacchioni S., Visca P.. ( 2006;). Burkholderia cepacia complex species: health hazards and biotechnological potential. Trends Microbiol14:277–286 [CrossRef][PubMed]
    [Google Scholar]
  10. 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 Immun70:1081–1086 [CrossRef][PubMed]
    [Google Scholar]
  11. Coyne C. B., Vanhook M. K., Gambling T. M., Carson J. L., Boucher R. C., Johnson L. G.. ( 2002;). Regulation of airway tight junctions by proinflammatory cytokines. Mol Biol Cell13:3218–3234 [CrossRef][PubMed]
    [Google Scholar]
  12. Cozens A. L., Yezzi M. J., Kunzelmann K., Ohrui T., Chin L., Eng K., Finkbeiner W. E., Widdicombe J. H., Gruenert D. C.. ( 1994;). CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol10:38–47[PubMed][CrossRef]
    [Google Scholar]
  13. Di Cello F., Bevivino A., Chiarini L., Fani R., Paffetti D., Tabacchioni S., Dalmastri C.. ( 1997;). Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microbiol63:4485–4493[PubMed]
    [Google Scholar]
  14. Drevinek P., Mahenthiralingam E.. ( 2010;). Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect16:821–830 [CrossRef][PubMed]
    [Google Scholar]
  15. Duff C., Murphy P. G., Callaghan M., McClean S.. ( 2006;). Differences in invasion and translocation of Burkholderia cepacia complex species in polarised lung epithelial cells in vitro. Microb Pathog41:183–192 [CrossRef][PubMed]
    [Google Scholar]
  16. Favia M., Guerra L., Fanelli T., Cardone R. A., Monterisi S., Di Sole F., Castellani S., Chen M., Seidler U.. & other authors ( 2010;). Na+/H+ exchanger regulatory factor 1 overexpression-dependent increase of cytoskeleton organization is fundamental in the rescue of F508del cystic fibrosis transmembrane conductance regulator in human airway CFBE41o− cells. Mol Biol Cell21:73–86 [CrossRef][PubMed]
    [Google Scholar]
  17. Goncz K. K., Feeney L., Gruenert D. C.. ( 1999;). Differential sensitivity of normal and cystic fibrosis airway epithelial cells to epinephrine. Br J Pharmacol128:227–233 [CrossRef][PubMed]
    [Google Scholar]
  18. Govan J. R., Deretic V.. ( 1996;). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia . Microbiol Rev60:539–574[PubMed]
    [Google Scholar]
  19. Gruenert D. C., Willems M., Cassiman J. J., Frizzell R. A.. ( 2004;). Established cell lines used in cystic fibrosis research. J Cyst Fibros3:Suppl. 2191–196 [CrossRef][PubMed]
    [Google Scholar]
  20. Guerra L., Fanelli T., Favia M., Riccardi S. M., Busco G., Cardone R. A., Carrabino S., Weinman E. J., Reshkin S. J.. & other authors ( 2005;). Na+/H+ exchanger regulatory factor isoform 1 overexpression modulates cystic fibrosis transmembrane conductance regulator (CFTR) expression and activity in human airway 16HBE14o− cells and rescues ΔF508 CFTR functional expression in cystic fibrosis cells. J Biol Chem280:40925–40933 [CrossRef][PubMed]
    [Google Scholar]
  21. Keig P. M., Ingham E., Vandamme P. A., Kerr K. G.. ( 2002;). Differential invasion of respiratory epithelial cells by members of the Burkholderia cepacia complex. Clin Microbiol Infect8:47–49 [CrossRef][PubMed]
    [Google Scholar]
  22. Kim J. Y., Sajjan U. S., Krasan G. P., LiPuma J. J.. ( 2005;). Disruption of tight junctions during traversal of the respiratory epithelium by Burkholderia cenocepacia . Infect Immun73:7107–7112 [CrossRef][PubMed]
    [Google Scholar]
  23. Kunzelmann K., Schwiebert E. M., Zeitlin P. L., Kuo W. L., Stanton B. A., Gruenert D. C.. ( 1993;). An immortalized cystic fibrosis tracheal epithelial cell line homozygous for the ΔF508 CFTR mutation. Am J Respir Cell Mol Biol8:522–529[PubMed][CrossRef]
    [Google Scholar]
  24. LeSimple P., Liao J., Robert R., Gruenert D. C., Hanrahan J. W.. ( 2010;). Cystic fibrosis transmembrane conductance regulator trafficking modulates the barrier function of airway epithelial cell monolayers. J Physiol588:1195–1209 [CrossRef][PubMed]
    [Google Scholar]
  25. LiPuma J. J., Spilker T., Coenye T., Gonzalez C. F.. ( 2002;). An epidemic Burkholderia cepacia complex strain identified in soil. Lancet359:2002–2003[CrossRef]
    [Google Scholar]
  26. Loutet S. A., Valvano M. A.. ( 2010;). A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun78:4088–4100 [CrossRef][PubMed]
    [Google Scholar]
  27. Magalhães M., de Britto M. C., Vandamme P.. ( 2002;). Burkholderia cepacia genomovar III and Burkholderia vietnamiensis double infection in a cystic fibrosis child. J Cyst Fibros1:292–294 [CrossRef][PubMed]
    [Google Scholar]
  28. Mahenthiralingam E., Vandamme P.. ( 2005;). Taxonomy and pathogenesis of the Burkholderia cepacia complex. Chron Respir Dis2:209–217 [CrossRef][PubMed]
    [Google Scholar]
  29. Mahenthiralingam E., Coenye T., Chung J. W., Speert D. P., Govan J. R. W., Taylor P., Vandamme P.. ( 2000;). Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol38:910–913[PubMed]
    [Google Scholar]
  30. Mahenthiralingam E., Baldwin A., Vandamme P.. ( 2002;). Burkholderia cepacia complex infection in patients with cystic fibrosis. J Med Microbiol51:533–538[PubMed]
    [Google Scholar]
  31. Mahenthiralingam E., Urban T. A., Goldberg J. B.. ( 2005;). The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol3:144–156 [CrossRef][PubMed]
    [Google Scholar]
  32. Mahenthiralingam E., Baldwin A., Dowson C. G.. ( 2008;). Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol104:1539–1551 [CrossRef][PubMed]
    [Google Scholar]
  33. Martin D. W., Mohr C. D.. ( 2000;). Invasion and intracellular survival of Burkholderia cepacia . Infect Immun68:24–29 [CrossRef][PubMed]
    [Google Scholar]
  34. McClean S., Callaghan M.. ( 2009;). Burkholderia cepacia complex: epithelial cell–pathogen confrontations and potential for therapeutic intervention. J Med Microbiol58:1–12 [CrossRef][PubMed]
    [Google Scholar]
  35. Nilsson H. E., Dragomir A., Lazorova L., Johannesson M., Roomans G. M.. ( 2010;). CFTR and tight junctions in cultured bronchial epithelial cells. Exp Mol Pathol88:118–127 [CrossRef][PubMed]
    [Google Scholar]
  36. Pirone L., Bragonzi A., Farcomeni A., Paroni M., Auriche C., Conese M., Chiarini L., Dalmastri C., Bevivino A., Ascenzioni F.. ( 2008;). Burkholderia cenocepacia strains isolated from cystic fibrosis patients are apparently more invasive and more virulent than rhizosphere strains. Environ Microbiol10:2773–2784 [CrossRef][PubMed]
    [Google Scholar]
  37. Reik R., Spilker T., Lipuma J. J.. ( 2005;). Distribution of Burkholderia cepacia complex species among isolates recovered from persons with or without cystic fibrosis. J Clin Microbiol43:2926–2928 [CrossRef][PubMed]
    [Google Scholar]
  38. Sajjan U., Keshavjee S., Forstner J.. ( 2004;). Responses of well-differentiated airway epithelial cell cultures from healthy donors and patients with cystic fibrosis to Burkholderia cenocepacia infection. Infect Immun72:4188–4199 [CrossRef][PubMed]
    [Google Scholar]
  39. Schwab U., Leigh M., Ribeiro C., Yankaskas J., Burns K., Gilligan P., Sokol P., Boucher R.. ( 2002;). Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect Immun70:4547–4555 [CrossRef][PubMed]
    [Google Scholar]
  40. Schwab U. E., Ribeiro C. M., Neubauer H., Boucher R. C.. ( 2003;). Role of actin filament network in Burkholderia multivorans invasion in well-differentiated human airway epithelia. Infect Immun71:6607–6609 [CrossRef][PubMed]
    [Google Scholar]
  41. Scordilis G. E., Ree H., Lessie T. G.. ( 1987;). Identification of transposable elements which activate gene expression in Pseudomonas cepacia . J Bacteriol169:8–13[PubMed]
    [Google Scholar]
  42. Speert D. P.. ( 2001;). Understanding Burkholderia cepacia: epidemiology, genomovars, and virulence. Infect Med18:49–56
    [Google Scholar]
  43. Speert D. P., Henry D., Vandamme P., Corey M., Mahenthiralingam E.. ( 2002;). Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis8:181–187[PubMed][CrossRef]
    [Google Scholar]
  44. Taylor J. B., Hogue L. A., LiPuma J. J., Walter M. J., Brody S. L., Cannon C. L.. ( 2010;). Entry of Burkholderia organisms into respiratory epithelium: CFTR, microfilament and microtubule dependence. J Cyst Fibros9:36–43 [CrossRef][PubMed]
    [Google Scholar]
  45. Umeda K., Ikenouchi J., Katahira-Tayama S., Furuse K., Sasaki H., Nakayama M., Matsui T., Tsukita S., Furuse M., Tsukita S.. ( 2006;). ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell126:741–754 [CrossRef][PubMed]
    [Google Scholar]
  46. Valvano M. A.. ( 2006;). Infections by Burkholderia spp.: the psychodramatic life of an opportunistic pathogen. Future Microbiol1:145–149 [CrossRef][PubMed]
    [Google Scholar]
  47. Vandamme P., Holmes B., Vancanneyt M., Coenye T., Hoste B., Coopman R., Revets H., Lauwers S., Gillis M.. & other authors ( 1997;). Occurrence of multiple genomovars of Burkholderia cepacia in cystic fibrosis patients and proposal of Burkholderia multivorans sp. nov.. Int J Syst Evol Microbiol47:1188–1200 [CrossRef][PubMed]
    [Google Scholar]
  48. Vandamme P., Holmes B., Coenye T., Goris J., Mahenthiralingam E., LiPuma J. J., Govan J. R.. ( 2003;). Burkholderia cenocepacia sp. nov.–a new twist to an old story. Res Microbiol154:91–96 [CrossRef][PubMed]
    [Google Scholar]
  49. Vanlaere E., LiPuma J. J., Baldwin A., Henry D., De Brandt E., Mahenthiralingam E., Speert D., Dowson C., Vandamme P.. ( 2008;). Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol58:1580–1590 [CrossRef][PubMed]
    [Google Scholar]
  50. Vanlaere E., Baldwin A., Gevers D., Henry D., De Brandt E., LiPuma J. J., Mahenthiralingam E., Speert D. P., Dowson C., Vandamme P.. ( 2009;). Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov.. Int J Syst Evol Microbiol59:102–111 [CrossRef][PubMed]
    [Google Scholar]
  51. Vial L., Groleau M. C., Lamarche M. G., Filion G., Castonguay-Vanier J., Dekimpe V., Daigle F., Charette S. J., Déziel E.. ( 2010;). Phase variation has a role in Burkholderia ambifaria niche adaptation. ISME J4:49–60 [CrossRef][PubMed]
    [Google Scholar]
  52. Vial L., Chapalain A., Groleau M. C., Déziel E.. ( 2011;). The various lifestyles of the Burkholderia cepacia complex species: a tribute to adaptation. Environ Microbiol13:1–12 [CrossRef][PubMed]
    [Google Scholar]
  53. Zelazny A. M., Ding L., Elloumi H. Z., Brinster L. R., Benedetti F., Czapiga M., Ulrich R. L., Ballentine S. J., Goldberg J. B.. & other authors ( 2009;). Virulence and cellular interactions of Burkholderia multivorans in chronic granulomatous disease. Infect Immun77:4337–4344 [CrossRef][PubMed]
    [Google Scholar]
  54. Zhang Y., Li X., Carpinteiro A., Gulbins E.. ( 2008;). Acid sphingomyelinase amplifies redox signaling in Pseudomonas aeruginosa-induced macrophage apoptosis. J Immunol181:4247–4254[PubMed][CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.056986-0
Loading
/content/journal/micro/10.1099/mic.0.056986-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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