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J. Biol. Chem., Vol. 279, Issue 41, 42984-42992, October 8, 2004
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From the
INSERM, EMI-0212 and ¶INSERM, U571 Faculté Necker Enfants Malades, 156 rue de Vaugirard, 75015 Paris and the **Institut National de la Recherche Agronomique, Unité d'Ecologie et de Physiologie du Systéme Digestif, 78350 Jouy-en-Josas, France
The capacity of non-pathogenic enteric bacteria to induce a pro-inflammatory response is under debate in terms of its effect on the symbiosis between the mammalian host and its commensal gut microflora. Activation of NF-
B and induction of interleukin-8 (IL-8) and CCL-20 by the commensal Escherichia coli strain MG1655 were first studied in vitro in the human intestinal epithelial cell (IECs) lines HT29-19A and Caco-2, transfected or not with plasmids encoding dominant negative Toll-like receptor (TLR) 5 and myeloid differentiation factor-88 (MyD88) adaptor protein. The response of enterocytes in situ was then assessed using murine ileal biopsies mounted in Ussing chambers. Commensal E. coli induced NF-B DNA binding, NF-B transcriptional activity, CCL-20 expression, and IL-8 secretion in the human IEC lines. E. coli MG1655 flagellin was necessary and sufficient to trigger this pro-inflammatory pathway via its interaction with TLR5 and the subsequent recruitment of the adaptor protein MyD88. Following epithelial cell polarization, signaling could be induced by live E. coli and flagellin on the apical side of HT29-19A. The in vivo relevance of our findings was confirmed, because immunohistochemical staining of murine ileum demonstrated expression of TLR5 in the apical part of enterocytes in situ. Furthermore, flagellin added on the mucosal side of murine ileal biopsies mounted in Ussing chambers induced a basolateral production of KC, a functional murine homolog of human IL-8. These findings provide strong evidence that flagellin released by flagellated commensal bacteria in the intestinal lumen can induce a pro-inflammatory response in enterocytes in vivo.
Received for publication, May 14, 2004 , and in revised form, July 8, 2004.
* This work was supported in part by INSERM, by Fondation Princesse Grace de Monaco, and by PTR Necker-Institut Pasteur 129. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Supported by a Ph.D. thesis fellowship from the Ministère de la Recherche.
|| Supported by a post-doctoral fellowship from La Ligue Contre le Cancer.
To whom correspondence should be addressed. Tel.: 33-1-40-61-53-02; Fax: 33-1-40-61-56-38; E-mail: gaboriau{at}necker.fr.
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