Virulence from vesicles: Novel mechanisms of host cell injury by Escherichia coli O104:H4 outbreak strain

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kunsmann, Lisa ^a   Rüter, Christian ^a   Bauwens, Andreas ^a   Greune, Lilo ^a   Glüder, Malte ^a   Kemper, Björn ^a   Fruth, Angelika ^b   Wai, Sun Nyunt ^c   He, Xiaohua ^d   Lloubes, Roland ^e   Schmidt, M Alexander ^a   Dobrindt, Ulrich ^a   Mellmann, Alexander ^a   Karch, Helge ^a   Bielaszewska, Martina ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

^c UMEÅ UNIVERSITY   (Sweden)

^d WESTERN REGIONAL RESEARCH CENTER   (United States)

^e CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; SHIGA TOXIN; SHIGA TOXIN SUBUNIT A; VIRULENCE FACTOR;

CACO-2 CELL LINE; CELL CULTURE; CLASSIFICATION; EPIDEMIC; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; EXOSOME; HT-29 CELL LINE; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; SPECIES DIFFERENCE;

BACTERIAL OUTER MEMBRANE PROTEINS; CACO-2 CELLS; CELLS, CULTURED; DISEASE OUTBREAKS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; EXTRACELLULAR VESICLES; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; SHIGA TOXIN; SPECIES SPECIFICITY; VIRULENCE FACTORS;

EID: 84939623832     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep13252     Document Type: Article

References (58)

1. Karch, H. et al. The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol. Med. 4, 841-848 (2012).
2. Bielaszewska, M. et al. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect. Dis. 11, 671-676 (2011).
3. Mellmann, A. et al. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS One 6, e22751 (2011).
4. Rasko, D. A. et al. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N. Engl. J. Med. 365, 709-717 (2011).
5. Zangari, T. et al. Virulence of the Shiga toxin type 2-expressing Escherichia coli O104:H4 German outbreak isolate in two animal models. Infect. Immun. 81, 1562-1574 (2013).
6. Zhang, W. et al. Lability of the pAA virulence plasmid in Escherichia coli O104:H4: Implications for virulence in humans. PLoS One 8, e66717 (2013).
7. Munera, D. et al. Autotransporters but not pAA are critical for rabbit colonization by Shiga toxin-producing Escherichia coli O104:H4. Nat. Commun. 5, 3080 (2014).
8. Boisen, N. et al. The presence of the pAA plasmid in the German O104:H4 Shiga toxin type 2a (Stx2a)-producing enteroaggregative Escherichia coli strain promotes the translocation of Stx2a across an epithelial cell monolayer. J. Infect. Dis. 210, 1909-1919 (2014).
9. Gerlach, R. G. & Hensel, M. Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int. J. Med. Microbiol. 297, 401-415 (2007).
10. Amano, A., Takeuchi, H. & Furuta, N. Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect. 12, 791-798 (2010).
11. Ellis, T. N. & Kuehn, M. J. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74, 81-94 (2010).
12. Bomberger, J. M. et al. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5, e1000382 (2009).
13. Kim, S. H. et al. Mouse model for hemolytic uremic syndrome induced by outer membrane vesicles of Escherichia coli O157:H7. FEMS Immunol. Med. Microbiol. 63, 427-434 (2011).
14. Bielaszewska, M. et al. Enterohemorrhagic Escherichia coli hemolysin employs outer membrane vesicles to target mitochondria and cause endothelial and epithelial apoptosis. PLoS Pathog. 9, e1003797 (2013).
15. Macia, E. et al. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell. 10, 839-850 (2006).
16. Wang, L. H., Rothberg, K. G. & Anderson, R. G. W. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. J. Cell. Biol. 123, 1107-1117 (1993).
17. Heuser, J. E. & Anderson, R. G. Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell. Biol. 108, 389-400 (1989).
18. Orlandi, P. A. & Fishman, P. H. Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell. Biol. 141, 905-915 (1998).
19. Rothberg, K. G., Ying, Y. S., Kamen, B. A. & Anderson, R. G. Cholesterol controls the clustering of the glycophospholipidanchored membrane receptor for 5-methyltetrahydrofolate. J. Cell. Biol. 111, 2931-2938 (1990).
20. Wadia, J. S., Stan, R. V. & Dowdy, S. F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nat. Med. 10, 310-315 (2004).
21. Konowalchuk, J., Speirs, J. I. & Stavric, S. Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 18, 775-779 (1977).
22. Jacewicz, M. S. et al. Maturational regulation of globotriaosylceramide, the Shiga-like toxin 1 receptor, in cultured human gut epithelial cells. J. Clin. Invest. 96, 1328-1335 (1995).
23. Schüller, S., Frankel, G. & Phillips, A. D. Interaction of Shiga toxin from Escherichia coli with human intestinal epithelial cell lines and explants: Stx2 induces epithelial damage in organ culture. Cell. Microbiol. 6, 289-301 (2004).
24. He, X., Patfield, S., Hnasko, R., Rasooly, R. & Mandrell, R. E. A polyclonal antibody based immunoassay detects seven subtypes of Shiga toxin 2 produced by Escherichia coli in human and environmental samples. PLoS One 8, e76368 (2013).
25. Khan, M. A., Kang, J. & Steiner, T. S. Enteroaggregative Escherichia coli flagellin-induced interleukin-8 secretion requires Toll-like receptor 5-dependent p38 MAP kinase activation. Immunology 112, 651-660 (2004).
26. Park, B. S. & Lee, J. O. Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp. Mol. Med. 45, e66 (2013).
27. Morrison, D. C. & Jacobs, D. M. Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides. Immunochemistry 13, 813-818 (1976).
28. Ellis, T. N., Leiman, S. A. & Kuehn, M. J. Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components. Infect. Immun. 78, 3822-3831 (2010).
29. Kolling, G. L. & Matthews, K. R. Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. App. Environ. Microbiol. 65, 1843-1848 (1999).
30. Waldor, M. K. & Friedman, D. I. Phage regulatory circuits and virulence gene expression. Curr. Opin. Microbiol. 8, 459-465 (2005).
31. Lingwood, C. A., Binnington, B., Manis, A. & Branch, D. R. Globotriaosyl ceramide receptor function - where membrane structure and pathology intersect. FEBS Lett. 584, 1879-1886 (2010).
32. Kovbasnjuk, O., Edidin, M. & Donowitz, M. Role of lipid rafts in Shiga toxin 1 interaction with the apical surface of Caco-2 cells. J. Cell. Sci. 114, 4025-4031 (2001).
33. Kovbasnjuk, O. et al. The glycosphingolipid globotriaosylceramide in the metastatic transformation of colon cancer. Proc. Natl. Acad. Sci. USA. 102, 19087-19092 (2005).
34. Kesty, N. C., Mason, K. M., Reedy, M., Miller, S. E. & Kuehn, M. J. Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 23, 4538-4549 (2004).
35. Chatterjee, D. & Chaudhuri, K. Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett. 585, 1357-1362 (2011).
36. Miyamoto, Y., Iimura, M., Kaper, J. B., Torres, A. G. & Kagnoff, M. F. Role of Shiga toxin versus H7 flagellin in enterohaemorrhagic Escherichia coli signalling of human colon epithelium in vivo. Cell. Microbiol. 8, 869-879 (2006).
37. Malyukova, I. et al. Macropinocytosis in Shiga toxin 1 uptake by human intestinal epithelial cells and transcellular transcytosis. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G78-92 (2009).
38. Tran, S. L., Billoud, L., Lewis, S. B., Phillips, A. D. & Schüller, S. Shiga toxin production and translocation during microaerobic human colonic infection with Shiga toxin-producing E. coli O157:H7 and O104:H4. Cell. Microbiol. 16, 1255-1266 (2014).
39. Hurley, B. P., Thorpe, C. M. & Acheson, D. W. Shiga toxin translocation across intestinal epithelial cells is enhanced by neutrophil transmigration. Infect. Immun. 69, 6148-6155 (2001).
40. Ståhl, A. L. et al. A novel mechanism of bacterial toxin transfer within host blood cell-derived microvesicles. PLoS Pathog. 11, e1004619 (2015).
41. Tesh, V. L. The induction of apoptosis by Shiga toxins and ricin. Curr. Top. Microbiol. Immunol. 357, 137-178 (2012).
42. Karpman, D. et al. Apoptosis of renal cortical cells in the hemolytic-uremic syndrome: in vivo and in vitro studies. Infect. Immun. 66, 636-644 (1998).
43. Porubsky, S. et al. Direct acute tubular damage contributes to Shiga toxin-mediated kidney failure. J. Pathol. 234, 120-133 (2014).
44. Berin, M. C., Darfeuille-Michaud, A., Egan, L. J., Miyamoto, Y. & Kagnoff, M. F. Role of EHEC O157:H7 virulence factors in the activation of intestinal epithelial cell NF-kappaB and MAP kinase pathways and the upregulated expression of interleukin 8. Cell. Microbiol. 4, 635-648 (2002).
45. Rogers, T. J., Paton, A. W., McColl, S. R. & Paton, J. C. Enhanced CXC chemokine responses of human colonic epithelial cells to locus of enterocyte effacement-negative shiga-toxigenic Escherichia coli. Infect. Immun. 71, 5623-5632 (2003).
46. Jandhyala, D. M. et al. Shiga toxin 2 and flagellin from shiga-toxigenic Escherichia coli superinduce interleukin-8 through synergistic effects on host stress-activated protein kinase activation. Infect. Immun. 78, 2984-2994 (2010).
47. Steiner, T. S., Nataro, J. P., Poteet-Smith, C. E., Smith, J. A. &, Guerrant, R. L. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J. Clin. Invest. 105, 1769-1777 (2000).
48. Thorpe, C. M. et al. Shiga toxins stimulate secretion of interleukin-8 from intestinal epithelial cells. Infect. Immun. 67, 5985-5993 (1999).
49. Strockbine, N. A. et al. Two toxin-converting phages from Escherichia coli O157:H7 strain 933 encode antigenically distinct toxins with similar biologic activities. Infect. Immun. 53, 135-140 (1986).
50. Ørskov, F. & Ørskov, I. Serotyping of Escherichia coli in Methods in Microbiology (ed. Bergan, T.) vol. 14, 43-112 (Academic Press, 1984).
51. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J. C. & Lloubes, R. Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J. Bacteriol. 184, 754-759 (2002).
52. Boisen, N., Ruiz-Perez, F., Scheutz, F., Krogfelt, K. A. & Nataro, J. P. Short report: high prevalence of serine protease autotransporter cytotoxins among strains of enteroaggregative Escherichia coli. Am. J. Trop. Med. Hyg. 80, 294-301 (2009).
53. Taylor, D. et al. Genome variability of O islands encoding tellurite resistance in enterohemorrhagic Escherichia coli O157:H7 isolates. J. Bacteriol. 184, 4690-4698 (2002).
54. Bauwens, A. et al. Differential cytotoxic actions of Shiga toxin 1 and Shiga toxin 2 on microvascular and macrovascular endothelial cells. Thromb. Haemost. 105, 515-528 (2011).
55. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F. & Riccardi, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide and flow cytometry. J. Immunol. Methods 139, 271-279 (1991).
56. Bielaszewska, M., Sinha, B., Kuczius, T. & Karch, H. Cytolethal distending toxin from Shiga toxin-producing Escherichia coli O157 causes irreversible G2/M arrest, inhibition of proliferation, and death of human endothelial cells. Infect. Immun. 73, 552-562 (2005).
57. Bettenworth, D. et al. Quantitative stain-free and continuous multimodal monitoring of wound healing in vitro with digital holographic microscopy. PLoS One 9, 07317 (2014).
58. Langehanenberg, P., von Bally, G. & Kemper, B. Autofocussing in digital holographic microscopy. 3D Res. 2, 01004 (2011).