1887

Abstract

causes a wide range of diseases from acute gastroenteritis to systemic typhoid fever, depending on the host. To invade non-phagocytic cells, has developed different mechanisms. The main invasion system requires a type III secretion system (T3SS) known as T3SS-1, which promotes a Trigger entry mechanism. However, other invasion factors have recently been described in , including Rck and PagN, which were not expressed under our bacterial culture conditions. Based on these observations, we used adhesion and invasion assays to analyse the respective roles of Enteritidis T3SS-1-dependent and -independent invasion processes at different times of infection. Diverse cell lines and cell types were tested, including endothelial, epithelial and fibroblast cells. We demonstrated that cell susceptibility to the T3SS-1-independent entry differs by a factor of nine between the most and the least permissive cell lines tested. In addition, using scanning electron and confocal microscopy, we showed that T3SS-1-independent entry into cells was characterized by a Trigger-like alteration, as for the T3SS-1-dependent entry, and also by Zipper-like cellular alteration. Our results demonstrate for what is believed to be the first time that can induce Trigger-like entry independently of T3SS-1 and can induce Zipper-like entry independently of Rck. Overall, these data open new avenues for discovering new invasion mechanisms in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.044941-0
2011-03-01
2019-12-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/3/839.html?itemId=/content/journal/micro/10.1099/mic.0.044941-0&mimeType=html&fmt=ahah

References

  1. Ahmer, B. M., van Reeuwijk, J., Timmers, C. D., Valentine, P. J. & Heffron, F. ( 1998; ). Salmonella Typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J Bacteriol 180, 1185–1193.
    [Google Scholar]
  2. Aiastui, A., Pucciarelli, M. G. & Garcia-del Portillo, F. ( 2010; ). Salmonella enterica serovar Typhimurium invades fibroblasts by multiple routes differing from the entry into epithelial cells. Infect Immun 78, 2700–2713.[CrossRef]
    [Google Scholar]
  3. Allen-Vercoe, E., Dibb-Fuller, M., Thorns, C. J. & Woodward, M. J. ( 1997; ). SEF17 fimbriae are essential for the convoluted colonial morphology of Salmonella Enteritidis. FEMS Microbiol Lett 153, 33–42.[CrossRef]
    [Google Scholar]
  4. Angot, A., Vergunst, A., Genin, S. & Peeters, N. ( 2007; ). Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathog 3, e3.[CrossRef]
    [Google Scholar]
  5. Coombes, B. K., Coburn, B. A., Potter, A. A., Gomis, S., Mirakhur, K., Li, Y. & Finlay, B. B. ( 2005; ). Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun 73, 7161–7169.[CrossRef]
    [Google Scholar]
  6. Cossart, P. & Sansonetti, P. J. ( 2004; ). Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 304, 242–248.[CrossRef]
    [Google Scholar]
  7. Datsenko, K. A. & Wanner, B. L. ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97, 6640–6645.[CrossRef]
    [Google Scholar]
  8. de Chastellier, C. & Berche, P. ( 1994; ). Fate of Listeria monocytogenes in murine macrophages: evidence for simultaneous killing and survival of intracellular bacteria. Infect Immun 62, 543–553.
    [Google Scholar]
  9. Delneste, Y., Beauvillain, C. & Jeannin, P. ( 2007; ). Innate immunity: structure and function of TLRs. Med Sci (Paris) 23, 67–73.[CrossRef]
    [Google Scholar]
  10. Desin, T. S., Lam, P. K., Koch, B., Mickael, C., Berberov, E., Wisner, A. L., Townsend, H. G., Potter, A. A. & Koster, W. ( 2009; ). Salmonella enterica serovar Enteritidis pathogenicity island 1 is not essential for but facilitates rapid systemic spread in chickens. Infect Immun 77, 2866–2875.[CrossRef]
    [Google Scholar]
  11. Fardini, Y., Chettab, K., Grepinet, O., Rochereau, S., Trotereau, J., Harvey, P., Amy, M., Bottreau, E., Bumstead, N. & other authors ( 2007; ). The YfgL lipoprotein is essential for type III secretion system expression and virulence of Salmonella enterica serovar Enteritidis. Infect Immun 75, 358–370.[CrossRef]
    [Google Scholar]
  12. Filloux, A., Hachani, A. & Bleves, S. ( 2008; ). The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154, 1570–1583.[CrossRef]
    [Google Scholar]
  13. Francis, C. L., Starnbach, M. N. & Falkow, S. ( 1992; ). Morphological and cytoskeletal changes in epithelial cells occur immediately upon interaction with Salmonella Typhimurium grown under low-oxygen conditions. Mol Microbiol 6, 3077–3087.[CrossRef]
    [Google Scholar]
  14. Hapfelmeier, S., Stecher, B., Barthel, M., Kremer, M., Müller, A. J., Heikenwalder, M., Stallmach, T., Hensel, M., Pfeffer, K. & other authors ( 2005; ). The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar Typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 174, 1675–1685.[CrossRef]
    [Google Scholar]
  15. Heithoff, D. M., Conner, C. P., Hanna, P. C., Julio, S. M., Hentschel, U. & Mahan, M. J. ( 1997; ). Bacterial infection as assessed by in vivo gene expression. Proc Natl Acad Sci U S A 94, 934–939.[CrossRef]
    [Google Scholar]
  16. Hu, Q., Coburn, B., Deng, W., Li, Y., Shi, X., Lan, Q., Wang, B., Coombes, B. K. & Finlay, B. B. ( 2008; ). Salmonella enterica serovar Senftenberg human clinical isolates lacking SPI-1. J Clin Microbiol 46, 1330–1336.[CrossRef]
    [Google Scholar]
  17. Khan, N. A., Kim, Y., Shin, S. & Kim, K. S. ( 2007; ). FimH-mediated Escherichia coli K1 invasion of human brain microvascular endothelial cells. Cell Microbiol 9, 169–178.[CrossRef]
    [Google Scholar]
  18. Kieda, C., Paprocka, M., Krawczenko, A., Zalecki, P., Dupuis, P., Monsigny, M., Radzikowski, C. & Dus, D. ( 2002; ). New human microvascular endothelial cell lines with specific adhesion molecules phenotypes. Endothelium 9, 247–261.[CrossRef]
    [Google Scholar]
  19. Kim, W. & Surette, M. G. ( 2006; ). Coordinated regulation of two independent cell-cell signaling systems and swarmer differentiation in Salmonella enterica serovar Typhimurium. J Bacteriol 188, 431–440.[CrossRef]
    [Google Scholar]
  20. Lambert, M. A. & Smith, S. G. ( 2008; ). The PagN protein of Salmonella enterica serovar Typhimurium is an adhesin and invasin. BMC Microbiol 8, 142.[CrossRef]
    [Google Scholar]
  21. Ly, K. T. & Casanova, J. E. ( 2007; ). Mechanisms of Salmonella entry into host cells. Cell Microbiol 9, 2103–2111.[CrossRef]
    [Google Scholar]
  22. Miao, E. A., Mao, D. P., Yudkovsky, N., Bonneau, R., Lorang, C. G., Warren, S. E., Leaf, I. A. & Aderem, A. ( 2010; ). Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci U S A 107, 3076–3080.[CrossRef]
    [Google Scholar]
  23. Rosselin, M., Virlogeux-Payant, I., Roy, C., Bottreau, E., Sizaret, P. Y., Mijouin, L., Germon, P., Caron, E., Velge, P. & Wiedemann, A. ( 2010; ). Rck of Salmonella enterica, subspecies enterica serovar Enteritidis, mediates Zipper-like internalization. Cell Res 20, 647–664.[CrossRef]
    [Google Scholar]
  24. Schmieger, H. ( 1999; ). Molecular survey of the Salmonella phage typing system of Anderson. J Bacteriol 181, 1630–1635.
    [Google Scholar]
  25. Velge, P., Bottreau, E., Kaeffer, B., Yurdusev, N., Pardon, P. & Van Langendonck, N. ( 1994; ). Protein tyrosine kinase inhibitors block the entries of Listeria monocytogenes and Listeria ivanovii into epithelial cells. Microb Pathog 17, 37–50.[CrossRef]
    [Google Scholar]
  26. Wallis, T. S. & Galyov, E. E. ( 2000; ). Molecular basis of Salmonella-induced enteritis. Mol Microbiol 36, 997–1005.[CrossRef]
    [Google Scholar]
  27. Wilson, J. W. & Nickerson, C. A. ( 2006; ). Cloning of a functional Salmonella SPI-1 type III secretion system and development of a method to create mutations and epitope fusions in the cloned genes. J Biotechnol 122, 147–160.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.044941-0
Loading
/content/journal/micro/10.1099/mic.0.044941-0
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