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Infection and Immunity, April 2004, p. 1896-1905, Vol. 72, No. 4
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.4.1896-1905.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Bovine Ileal Intraepithelial Lymphocytes Represent Target Cells for Shiga Toxin 1 from Escherichia coli

Christian Menge,* Maike Blessenohl, Tobias Eisenberg, Ivonne Stamm, and Georg Baljer

Institut für Hygiene und Infektionskrankheiten der Tiere der Justus-Liebig-Universität Giessen, D-35392 Giessen, Germany

Received 25 July 2003/ Returned for modification 9 October 2003/ Accepted 8 January 2004

The discovery that bovine peripheral lymphocytes are sensitive to Stx1 identified a possible mechanism for the persistence of infections with Shiga toxin (Stx)-producing Escherichia coli (STEC) in the bovine reservoir host. If intraepithelial lymphocytes (IEL) are also sensitive to Stx1, the idea that Stx1 affects inflammation in the bovine intestine is highly attractive. To prove this hypothesis, ileal IEL (iIEL) were prepared from adult cattle, characterized by flow cytometry, and subjected to functional assays in the presence and absence of purified Stx1. We found that 14.9% of all iIEL expressed Gb3/CD77, the Stx1 receptor on bovine lymphocytes, and 7.9% were able to bind the recombinant B subunit of Stx1. The majority of Gb3/CD77+ cells were activated CD3+ CD6+ CD8{alpha}+ T cells, whereas only some CD4+ T cells and B cells expressed Gb3/CD77. However, Stx1 blocked the mitogen-induced transformation to enlarged blast cells within all subpopulations to a similar extent and significantly reduced the percentage of Gb3/CD77+ cells. Although Stx1 did not affect the natural killer cell activity of iIEL, the toxin accelerated the synthesis of interleukin-4 (IL-4) mRNA and reduced the amount of IL-8 mRNA in bovine iIEL cultures. Because the intestinal system comprises a rich network of interactions between different types of cells and any dysfunction may influence the course of intestinal infections, this demonstration that Stx1 can target bovine IEL may be highly relevant for our understanding of the interplay between STEC and its reservoir host.

* Corresponding author. Mailing address: Institut für Hygiene und Infektionskrankheiten der Tiere, Frankfurter Str. 89, D-35392 Giessen, Germany. Phone: 49-641-99-38314. Fax: 49-641-99-38309. E-mail: christian.menge{at}vetmed.uni-giessen.de.

Editor: A. D. O'Brien

Infection and Immunity, April 2004, p. 1896-1905, Vol. 72, No. 4
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.4.1896-1905.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Frohlich, J., Baljer, G., Menge, C. (2009). Maternally and Naturally Acquired Antibodies to Shiga Toxins in a Cohort of Calves Shedding Shiga-Toxigenic Escherichia coli. Appl. Environ. Microbiol. 75: 3695-3704 [Abstract] [Full Text]  
  • Meltz Steinberg, K., Levin, B. R (2007). Grazing protozoa and the evolution of the Escherichia coli O157:H7 Shiga toxin-encoding prophage. Proc R Soc B 274: 1921-1929 [Abstract] [Full Text]  
  • Cornick, N. A., Helgerson, A. F., Sharma, V. (2007). Shiga Toxin and Shiga Toxin-Encoding Phage Do Not Facilitate Escherichia coli O157:H7 Colonization in Sheep. Appl. Environ. Microbiol. 73: 344-346 [Abstract] [Full Text]  
  • Hoffman, M. A., Menge, C., Casey, T. A., Laegreid, W., Bosworth, B. T., Dean-Nystrom, E. A. (2006). Bovine Immune Response to Shiga-Toxigenic Escherichia coli O157:H7. CVI 13: 1322-1327 [Abstract] [Full Text]  
  • Menge, C., Stamm, I., van Diemen, P. M., Sopp, P., Baljer, G., Wallis, T. S., Stevens, M. P. (2004). Phenotypic and functional characterization of intraepithelial lymphocytes in a bovine ligated intestinal loop model of enterohaemorrhagic Escherichia coli infection. J Med Microbiol 53: 573-579 [Abstract] [Full Text]  


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