Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli
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....
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00742/full |
| _version_ | 1811323930207584256 |
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| author | Tetiana Dumych Nao Yamakawa Adeline Sivignon Estelle Garenaux Stefania Robakiewicz Bernadette Coddeville Antonino Bongiovanni Fabrice Bray Nicolas Barnich Sabine Szunerits Christian Slomianny Martin Herrmann Sébastien G. Gouin Alexander D. Lutsyk Luis E. Munoz Frank Lafont Christian Rolando Rostyslav Bilyy Julie M. J. Bouckaert |
| author_facet | Tetiana Dumych Nao Yamakawa Adeline Sivignon Estelle Garenaux Stefania Robakiewicz Bernadette Coddeville Antonino Bongiovanni Fabrice Bray Nicolas Barnich Sabine Szunerits Christian Slomianny Martin Herrmann Sébastien G. Gouin Alexander D. Lutsyk Luis E. Munoz Frank Lafont Christian Rolando Rostyslav Bilyy Julie M. J. Bouckaert |
| author_sort | Tetiana Dumych |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T14:05:19Z |
| format | Article |
| id | doaj.art-3d043b28b2414895a5dff9140868b553 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T14:05:19Z |
| publishDate | 2018-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-3d043b28b2414895a5dff9140868b5532022-12-22T02:43:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-04-01910.3389/fmicb.2018.00742323098Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coliTetiana Dumych0Nao Yamakawa1Adeline Sivignon2Estelle Garenaux3Stefania Robakiewicz4Bernadette Coddeville5Antonino Bongiovanni6Fabrice Bray7Nicolas Barnich8Sabine Szunerits9Christian Slomianny10Martin Herrmann11Sébastien G. Gouin12Alexander D. Lutsyk13Luis E. Munoz14Frank Lafont15Christian Rolando16Rostyslav Bilyy17Julie M. J. Bouckaert18Department of Histology, Cytology and Embryology, Danylo Halytsky Lviv National Medical University, Lviv, UkraineUnité de Glycobiologie Structurale et Fonctionnelle, UMR8576 Centre National de la Recherche Scientifique, University of Lille, Villeneuve d'Ascq, FranceUniversité Clermont Auvergne, Institut National de la Santé et de la Recherche Médicale U1071, USC-INRA 2018, M2iSH, Clermont-Ferrand, FranceUniversité Clermont Auvergne, Institut National de la Santé et de la Recherche Médicale U1071, USC-INRA 2018, M2iSH, Clermont-Ferrand, FranceUnité de Glycobiologie Structurale et Fonctionnelle, UMR8576 Centre National de la Recherche Scientifique, University of Lille, Villeneuve d'Ascq, FranceUnité de Glycobiologie Structurale et Fonctionnelle, UMR8576 Centre National de la Recherche Scientifique, University of Lille, Villeneuve d'Ascq, FranceCellular Microbiology and Physics of Infection Group-Center of Infection and Immunity of Lille, Institut Pasteur de Lille, Centre National de la Recherche Scientifique UMR8204, INSERM U1019, Lille Regional Hospital University Centre, University of Lille, Lille, FranceMiniaturisation pour l'Analyse, la Synthèse et la Protéomique, USR 3290 Centre National de la Recherche Scientifique, University of Lille, Villeneuve d'Ascq, FranceUniversité Clermont Auvergne, Institut National de la Santé et de la Recherche Médicale U1071, USC-INRA 2018, M2iSH, Clermont-Ferrand, FranceInstitut Supérieur de l'Electronique et du Numérique, University of Lille, Centrale Lille, UMR 8520—IEMN, University Valenciennes, Lille, FranceLaboratoire de Physiologie Cellulaire, Institut National de la Santé et de la Recherche Médicale U.1003, University of Lille, Villeneuve d'Ascq, FranceDepartment of Internal Medicine 3—Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nürnberg and Universitätsklinikum Erlangen, Erlangen, GermanyChimie Et Interdisciplinarité, Synthèse, Analyse, Modélisation, UMR 6230 Centre National de la Recherche Scientifique, Université Nantes Angers Le Mans (L'UNAM), Nantes, FranceDepartment of Histology, Cytology and Embryology, Danylo Halytsky Lviv National Medical University, Lviv, UkraineDepartment of Internal Medicine 3—Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nürnberg and Universitätsklinikum Erlangen, Erlangen, GermanyCellular Microbiology and Physics of Infection Group-Center of Infection and Immunity of Lille, Institut Pasteur de Lille, Centre National de la Recherche Scientifique UMR8204, INSERM U1019, Lille Regional Hospital University Centre, University of Lille, Lille, FranceMiniaturisation pour l'Analyse, la Synthèse et la Protéomique, USR 3290 Centre National de la Recherche Scientifique, University of Lille, Villeneuve d'Ascq, FranceDepartment of Histology, Cytology and Embryology, Danylo Halytsky Lviv National Medical University, Lviv, UkraineUnité de Glycobiologie Structurale et Fonctionnelle, UMR8576 Centre National de la Recherche Scientifique, University of Lille, Villeneuve d'Ascq, FranceA 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.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00742/fullCEACAM6adherent-invasive E. coliapoptotic cell-derived membranous vesiclesoligomannose glycansCrohn's disease |
| spellingShingle | Tetiana Dumych Nao Yamakawa Adeline Sivignon Estelle Garenaux Stefania Robakiewicz Bernadette Coddeville Antonino Bongiovanni Fabrice Bray Nicolas Barnich Sabine Szunerits Christian Slomianny Martin Herrmann Sébastien G. Gouin Alexander D. Lutsyk Luis E. Munoz Frank Lafont Christian Rolando Rostyslav Bilyy Julie M. J. Bouckaert Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli Frontiers in Microbiology CEACAM6 adherent-invasive E. coli apoptotic cell-derived membranous vesicles oligomannose glycans Crohn's disease |
| title | Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli |
| title_full | Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli |
| title_fullStr | Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli |
| title_full_unstemmed | Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli |
| title_short | Oligomannose-Rich Membranes of Dying Intestinal Epithelial Cells Promote Host Colonization by Adherent-Invasive E. coli |
| title_sort | oligomannose rich membranes of dying intestinal epithelial cells promote host colonization by adherent invasive e coli |
| topic | CEACAM6 adherent-invasive E. coli apoptotic cell-derived membranous vesicles oligomannose glycans Crohn's disease |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00742/full |
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