1887

Abstract

is an opportunistic human pathogen associated with immunosuppressed people. While the interaction of with macrophages has been comprehensively studied, little is known about its interactions with non-phagocytic cells. Here, we characterized the entry process of this bacterium into human lung epithelial cells. The invasion is inhibited by nocodazole and wortmannin, suggesting that the phosphatidylinositol 3-kinase pathway and microtubule cytoskeleton are important for invasion. Pre-incubation of with a rabbit anti polyclonal antiserum resulted in a dramatic reduction in invasion. Also, the invasion process as studied by immunofluorescence and scanning electron microscopy indicates that make initial contact with the microvilli of the A549 cells, and at the structural level, the entry process was observed to occur via a zipper-like mechanism. Infected lung epithelial cells upregulate the expression of cytokines IL-8 and IL-6 upon infection. The production of these pro-inflammatory cytokines was significantly enhanced in culture supernatants from cells infected with non-mucoid plasmid-less strains when compared with cells infected with mucoid strains. These results demonstrate that human airway epithelial cells produce pro-inflammatory mediators against isolates.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.056234-0
2013-08-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jmm/62/8/1144.html?itemId=/content/journal/jmm/10.1099/jmm.0.056234-0&mimeType=html&fmt=ahah

References

  1. Al Akhrass F., Al Wohoush I., Chaftari A. M., Reitzel R., Jiang Y., Ghannoum M., Tarrand J., Hachem R., Raad I. 2012; Rhodococcus bacteremia in cancer patients is mostly catheter related and associated with biofilm formation. PLoS ONE 7:e32945 [View Article][PubMed]
    [Google Scholar]
  2. Andersen C., Rak B., Benz R. 1999; The gene bglH present in the bgl operon of Escherichia coli, responsible for uptake and fermentation of beta-glucosides encodes for a carbohydrate-specific outer membrane porin. Mol Microbiol 31:499–510 [View Article][PubMed]
    [Google Scholar]
  3. Bertuccini L., Baldassarri L., von Hunolstein C. 2004; Internalization of non-toxigenic Corynebacterium diphtheriae by cultured human respiratory epithelial cells. Microb Pathog 37:111–118 [View Article][PubMed]
    [Google Scholar]
  4. Byrne B. A., Prescott J. F., Palmer G. H., Takai S., Nicholson V. M., Alperin D. C., Hines S. A. 2001; Virulence plasmid of Rhodococcus equi contains inducible gene family encoding secreted proteins. Infect Immun 69:650–656 [View Article][PubMed]
    [Google Scholar]
  5. Copeland K. F. 2005; Modulation of HIV-1 transcription by cytokines and chemokines. Mini Rev Med Chem 5:1093–1101 [View Article][PubMed]
    [Google Scholar]
  6. Corti M., Palmero D., Eiguchi K. 2009; Respiratory infections in immunocompromised patients. Curr Opin Pulm Med 15:209–217 [View Article][PubMed]
    [Google Scholar]
  7. Cossart P., Sansonetti P. J. 2004; Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304:242–248 [View Article][PubMed]
    [Google Scholar]
  8. Cossart P., Toledo-Arana A. 2008; Listeria monocytogenes, a unique model in infection biology: an overview. Microbes Infect 10:1041–1050 [View Article][PubMed]
    [Google Scholar]
  9. Cromwell O., Hamid Q., Corrigan C. J., Barkans J., Meng Q., Collins P. D., Kay A. B. 1992; Expression and generation of interleukin-8, IL-6 and granulocyte-macrophage colony-stimulating factor by bronchial epithelial cells and enhancement by IL-1β and tumour necrosis factor-α. Immunology 77:330–337[PubMed]
    [Google Scholar]
  10. Dann S. M., Spehlmann M. E., Hammond D. C., Iimura M., Hase K., Choi L. J., Hanson E., Eckmann L. 2008; IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol 180:6816–6826[PubMed] [CrossRef]
    [Google Scholar]
  11. de la Peña-Moctezuma A., Prescott J. F. 1995; A physical map of the 85 kb virulence plasmid of Rhodococcus equi 103. Can J Vet Res 59:229–231[PubMed]
    [Google Scholar]
  12. Doran K. S., Chang J. C., Benoit V. M., Eckmann L., Nizet V. 2002; Group B streptococcal beta-hemolysin/cytolysin promotes invasion of human lung epithelial cells and the release of interleukin-8. J Infect Dis 185:196–203 [View Article][PubMed]
    [Google Scholar]
  13. Dube P. H., Handley S. A., Lewis J., Miller V. L. 2004; Protective role of interleukin-6 during Yersinia enterocolitica infection is mediated through the modulation of inflammatory cytokines. Infect Immun 72:3561–3570 [View Article][PubMed]
    [Google Scholar]
  14. Fernandez-Mora E., Polidori M., Lührmann A., Schaible U. E., Haas A. 2005; Maturation of Rhodococcus equi-containing vacuoles is arrested after completion of the early endosome stage. Traffic 6:635–653 [View Article][PubMed]
    [Google Scholar]
  15. Frick A. G., Joseph T. D., Pang L., Rabe A. M., St Geme J. W. III, Look D. C. 2000; Haemophilus influenzae stimulates ICAM-1 expression on respiratory epithelial cells. J Immunol 164:4185–4196[PubMed] [CrossRef]
    [Google Scholar]
  16. Giguère S., Prescott J. F. 1998; Cytokine induction in murine macrophages infected with virulent and avirulent Rhodococcus equi . Infect Immun 66:1848–1854[PubMed]
    [Google Scholar]
  17. Hoffmann E., Dittrich-Breiholz O., Holtmann H., Kracht M. 2002; Multiple control of interleukin-8 gene expression. J Leukoc Biol 72:847–855[PubMed]
    [Google Scholar]
  18. Isberg R. R., Falkow S. 1985; A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317:262–264 [View Article][PubMed]
    [Google Scholar]
  19. Kanaly S. T., Hines S. A., Palmer G. H. 1996; Transfer of a CD4+ Th1 cell line to nude mice effects clearance of Rhodococcus equi from the lung. Infect Immun 64:1126–1132[PubMed]
    [Google Scholar]
  20. Kaplanski G., Teysseire N., Farnarier C., Kaplanski S., Lissitzky J. C., Durand J. M., Soubeyrand J., Dinarello C. A., Bongrand P. 1995; IL-6 and IL-8 production from cultured human endothelial cells stimulated by infection with Rickettsia conorii via a cell-associated IL-1 α-dependent pathway. J Clin Invest 96:2839–2844 [View Article][PubMed]
    [Google Scholar]
  21. Madigan J. E., Hietala S., Muller N. 1991; Protection against naturally acquired Rhodococcus equi pneumonia in foals by administration of hyperimmune plasma. J Reprod Fertil Suppl 44:571–578[PubMed]
    [Google Scholar]
  22. Maza P. K., Oliveira P., Toledo M. S., Paula D. M., Takahashi H. K., Straus A. H., Suzuki E. 2012; Paracoccidioides brasiliensis induces secretion of IL-6 and IL-8 by lung epithelial cells. Modulation of host cytokine levels by fungal proteases. Microbes Infect 14:1077–1085 [View Article][PubMed]
    [Google Scholar]
  23. Misawa N., Blaser M. J. 2000; Detection and characterization of autoagglutination activity by Campylobacter jejuni . Infect Immun 68:6168–6175 [View Article][PubMed]
    [Google Scholar]
  24. Molinari G., Rohde M., Guzmán C. A., Chhatwal G. S. 2000; Two distinct pathways for the invasion of Streptococcus pyogenes in non-phagocytic cells. Cell Microbiol 2:145–154 [View Article][PubMed]
    [Google Scholar]
  25. Nitsche-Schmitz D. P., Rohde M., Chhatwal G. S. 2007; Invasion mechanisms of Gram-positive pathogenic cocci. Thromb Haemost 98:488–496[PubMed]
    [Google Scholar]
  26. O’Toole G. A., Kolter R. 1998; Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461 [View Article][PubMed]
    [Google Scholar]
  27. Ocampo-Sosa A. A., Lewis D. A., Navas J., Quigley F., Callejo R., Scortti M., Leadon D. P., Fogarty U., Vazquez-Boland J. A. 2007; Molecular epidemiology of Rhodococcus equi based on traA, vapA, and vapB virulence plasmid markers. J Infect Dis 196:763–769 [View Article][PubMed]
    [Google Scholar]
  28. Okuda J., Hayashi N., Tanabe S., Minagawa S., Gotoh N. 2011; Degradation of interleukin 8 by the serine protease MucD of Pseudomonas aeruginosa . J Infect Chemother 17:782–792 [View Article][PubMed]
    [Google Scholar]
  29. Paula S. J., Duffey P. S., Abbott S. L., Kokka R. P., Oshiro L. S., Janda J. M., Shimada T., Sakazaki R. 1988; Surface properties of autoagglutinating mesophilic aeromonads. Infect Immun 56:2658–2665[PubMed]
    [Google Scholar]
  30. Pilares L., Agüero J., Vázquez-Boland J. A., Martínez-Martínez L., Navas J. 2010; Identification of atypical Rhodococcus-like clinical isolates as Dietzia spp. by 16S rRNA gene sequencing. J Clin Microbiol 48:1904–1907 [View Article][PubMed]
    [Google Scholar]
  31. Pittet J. F., Mackersie R. C., Martin T. R., Matthay M. A. 1997; Biological markers of acute lung injury: prognostic and pathogenetic significance. Am J Respir Crit Care Med 155:1187–1205 [View Article][PubMed]
    [Google Scholar]
  32. Ramos-Vivas J., Pilares-Ortega L., Remuzgo-Martínez S., Padilla D., Gutiérrez-Díaz J. L., Navas-Méndez J. 2011; Rhodococcus equi human clinical isolates enter and survive within human alveolar epithelial cells. Microbes Infect 13:438–446 [View Article][PubMed]
    [Google Scholar]
  33. Roggenkamp A., Neuberger H. R., Flügel A., Schmoll T., Heesemann J. 1995; Substitution of two histidine residues in YadA protein of Yersinia enterocolitica abrogates collagen binding, cell adherence and mouse virulence. Mol Microbiol 16:1207–1219 [View Article][PubMed]
    [Google Scholar]
  34. Sukumaran S. K., Quon M. J., Prasadarao N. V. 2002; Escherichia coli K1 internalization via caveolae requires caveolin-1 and protein kinase Cα interaction in human brain microvascular endothelial cells. J Biol Chem 277:50716–50724 [View Article][PubMed]
    [Google Scholar]
  35. Swanson J., Kraus S. J., Gotschlich E. C. 1971; Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med 134:886–906 [View Article][PubMed]
    [Google Scholar]
  36. Taylor R. K., Miller V. L., Furlong D. B., Mekalanos J. J. 1987; Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc Natl Acad Sci U S A 84:2833–2837 [View Article][PubMed]
    [Google Scholar]
  37. Topino S., Galati V., Grilli E., Petrosillo N. 2010; Rhodococcus equi infection in HIV-infected individuals: case reports and review of the literature. AIDS Patient Care STDS 24:211–222 [View Article][PubMed]
    [Google Scholar]
  38. van Faassen H., KuoLee R., Harris G., Zhao X., Conlan J. W., Chen W. 2007; Neutrophils play an important role in host resistance to respiratory infection with Acinetobacter baumannii in mice. Infect Immun 75:5597–5608 [View Article][PubMed]
    [Google Scholar]
  39. von Bargen K., Haas A. 2009; Molecular and infection biology of the horse pathogen Rhodococcus equi . FEMS Microbiol Rev 33:870–891 [View Article][PubMed]
    [Google Scholar]
  40. Weinstock D. M., Brown A. E. 2002; Rhodococcus equi: an emerging pathogen. Clin Infect Dis 34:1379–1385 [View Article][PubMed]
    [Google Scholar]
  41. Wiersinga W. J., van der Poll T., White N. J., Day N. P., Peacock S. J. 2006; Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei . Nat Rev Microbiol 4:272–282 [View Article][PubMed]
    [Google Scholar]
  42. Yamshchikov A. V., Schuetz A., Lyon G. M. 2010; Rhodococcus equi infection. Lancet Infect Dis 10:350–359 [View Article][PubMed]
    [Google Scholar]
  43. Yang J., Hooper W. C., Phillips D. J., Talkington D. F. 2002; Regulation of proinflammatory cytokines in human lung epithelial cells infected with Mycoplasma pneumoniae . Infect Immun 70:3649–3655 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.056234-0
Loading
/content/journal/jmm/10.1099/jmm.0.056234-0
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