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Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli

Tetiana Dumych 1 Nao Yamakawa 1 Adeline Sivignon 2 Estelle Garénaux 1, 2 Stefania Robakiewicz Bernadette Coddeville 1 Antonino Bongiovanni 3 Fabrice Bray Nicolas Barnich 2 Sabine Szunerits 4, 5 Christian Slomianny 6 Martin Herrmann Sébastien Gouin 7 Alexander Lutsyk Luis Munoz 8 Frank Lafont 9 Christian Rolando 10 Rostyslav Bilyy 11 Julie Bouckaert 1
1 UGSF - Unité de Glycobiologie Structurale et Fonctionnelle UMR 8576
2 M2iSH - Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte
3 Institut Fédératif de Recherche 142
4 IEMN - Institut d’Électronique, de Microélectronique et de Nanotechnologie - UMR 8520
5 NBI - IEMN - NanoBioInterfaces - IEMN
IEMN - Institut d’Électronique, de Microélectronique et de Nanotechnologie - UMR 8520
6 Rôle des canaux ioniques membranaires et du calcium intracellulaire dans la physiopathologie de la prostate
7 LSOHOOM - Laboratoire de Synthèse Organique (Hétérochimie organique, organoéléments et matériaux)
8 Universidad de Cantabria [Santander]
9 IBL - Bioimaging platform
10 UMR CNRS 8009 - Laboratoire de Chimie Organique et Macromoleculaire
11 Danylo Halytskiy Lviv National Medical University
Abstract : A novel mechanism is revealed by which clinical isolates of adherent-invasive Escherichia coli (AIEC) penetrate into the epithelial cell layer, replicate, and establish biofilms in Crohn's disease. AIEC uses the FimH fimbrial adhesin to bind to oligomannose glycans on the surface of host cells. Oligomannose glycans exposed on early apoptotic cells are the preferred binding targets of AIEC, so apoptotic cells serve as potential entry points for bacteria into the epithelial cell layer. Thereafter, the bacteria propagate laterally in the epithelial intercellular spaces. We demonstrate oligomannosylation at two distinct sites of a glycoprotein receptor for AIEC, carcinoembryonic antigen related cell adhesion molecule 6 (CEACAM6 or CD66c), on human intestinal epithelia. After bacterial binding, FimH interacts with CEACAM6, which then clusters. The presence of the highest-affinity epitope for FimH, oligomannose-5, on CEACAM6 is demonstrated using LC-MS/MS. As mannose-dependent infections are abundant, this mechanism might also be used by other adherent-invasive pathogens.
Keywords : apoptotic cell-derived membranous vesicles adherent-invasive E coli CEACAM6 Crohn's disease oligomannose glycans
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Submitted on : Thursday, November 15, 2018 - 3:50:55 PM
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Tetiana Dumych, Nao Yamakawa, Adeline Sivignon, Estelle Garénaux, Stefania Robakiewicz, et al.. Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli. Frontiers in Microbiology, Frontiers Media, 2018, 9, ⟨10.3389/fmicb.2018.00742⟩. ⟨hal-01796957⟩

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