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Infection and Immunity, November 2008, p. 5381-5391, Vol. 76, No. 11
0019-9567/08/$08.00+0     doi:10.1128/IAI.00553-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Epithelial and Mesenchymal Cells in the Bovine Colonic Mucosa Differ in Their Responsiveness to Escherichia coli Shiga Toxin 1

Ivonne Stamm,¹ Melanie Mohr,¹ Philip S. Bridger,¹ Elmar Schröpfer,¹ Matthias König,² William C. Stoffregen,³ Evelyn A. Dean-Nystrom,³ Georg Baljer,¹ and Christian Menge^1*

Institut für Hygiene und Infektionskrankheiten der Tiere,¹ Institut für Virologie, Justus-Liebig-Universität, D-35392 Giessen, Germany,² Pre-Harvest Food Safety and Enteric Diseases Research, National Animal Disease Center, USDA, Agriculture Research Service, Ames, Iowa 50010³

Received 6 May 2008/ Returned for modification 19 June 2008/ Accepted 26 August 2008

Bovine colonic crypt cells express CD77 molecules that potentially act as receptors for Shiga toxins (Stx). The implication of this finding for the intestinal colonization of cattle by human pathogenic Stx-producing Escherichia coli (STEC) remains undefined. We used flow cytometric and real-time PCR analyses of primary cultures of colonic crypt cells to evaluate cell viability, CD77 expression, and gene transcription in the presence and absence of purified Stx1. A subset of cultured epithelial cells had Stx receptors which were located mainly intracellularly, with a perinuclear distribution, and were resistant to Stx1-induced apoptosis and Stx1 effects on chemokine expression patterns. In contrast, a population of vimentin-positive cells, i.e., mesenchymal/nonepithelial cells that had high numbers of Stx receptors on their surface, was depleted from the cultures by Stx1. In situ, CD77⁺ cells were located in the lamina propria of the bovine colon by using immunofluorescence staining. A newly established vimentin-positive crypt cell line with high CD77 expression resisted the cytolethal effect of Stx1 but responded to Stx1 with a significant increase in interleukin-8 (IL-8), GRO-, MCP-1, and RANTES mRNA. Combined stimulation with lipopolysaccharide and Stx1 increased IL-10 mRNA. Our results show that bovine colonic crypt cells of epithelial origin are resistant to both the cytotoxic and modulatory effects of Stx1. In contrast, some mucosal mesenchymal cells, preliminarily characterized as mucosal macrophages, are Stx1-responsive cells that may participate in the interaction of STEC with the bovine intestinal mucosa.

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* Corresponding author. Mailing address: Institut für Hygiene und Infektionskrankheiten der Tiere, Frankfurter Strasse 85-89, D-35392 Giessen, Germany. Phone: 49-641-99-38314. Fax: 49-641-99-38309. E-mail: christian.menge{at}vetmed.uni-giessen.de

Published ahead of print on 2 September 2008.

Editor: S. R. Blanke

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Infection and Immunity, November 2008, p. 5381-5391, Vol. 76, No. 11
0019-9567/08/$08.00+0     doi:10.1128/IAI.00553-08
Copyright © 2008, 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]