Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.

Adherent-invasive Escherichia coli (AIEC) are abnormally predominant on Crohn's disease (CD) ileal mucosa. AIEC reference strain LF82 adheres to ileal enterocytes via the common type 1 pili adhesin FimH and recognizes CEACAM6 receptors abnormally expressed on CD ileal epithelial cells. The fimH...

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Autores principales:	Nicolas Dreux, Jérémy Denizot, Margarita Martinez-Medina, Alexander Mellmann, Maria Billig, Dagmara Kisiela, Sujay Chattopadhyay, Evgeni Sokurenko, Christel Neut, Corinne Gower-Rousseau, Jean-Frédéric Colombel, Richard Bonnet, Arlette Darfeuille-Michaud, Nicolas Barnich
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2013
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/e4669ff6ea7c4a89b4023b6ba16045c3
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spelling	oai:doaj.org-article:e4669ff6ea7c4a89b4023b6ba16045c32021-11-18T06:06:08ZPoint mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.1553-73661553-737410.1371/journal.ppat.1003141https://doaj.org/article/e4669ff6ea7c4a89b4023b6ba16045c32013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23358328/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Adherent-invasive Escherichia coli (AIEC) are abnormally predominant on Crohn's disease (CD) ileal mucosa. AIEC reference strain LF82 adheres to ileal enterocytes via the common type 1 pili adhesin FimH and recognizes CEACAM6 receptors abnormally expressed on CD ileal epithelial cells. The fimH genes of 45 AIEC and 47 non-AIEC strains were sequenced. The phylogenetic tree based on fimH DNA sequences indicated that AIEC strains predominantly express FimH with amino acid mutations of a recent evolutionary origin - a typical signature of pathoadaptive changes of bacterial pathogens. Point mutations in FimH, some of a unique AIEC-associated nature, confer AIEC bacteria a significantly higher ability to adhere to CEACAM-expressing T84 intestinal epithelial cells. Moreover, in the LF82 strain, the replacement of fimH(LF82) (expressing FimH with an AIEC-associated mutation) with fimH(K12) (expressing FimH of commensal E. coli K12) decreased the ability of bacteria to persist and to induce severe colitis and gut inflammation in infected CEABAC10 transgenic mice expressing human CEACAM receptors. Our results highlight a mechanism of AIEC virulence evolution that involves selection of amino acid mutations in the common bacterial traits, such as FimH protein, and leads to the development of chronic inflammatory bowel disease (IBD) in a genetically susceptible host. The analysis of fimH SNPs may be a useful method to predict the potential virulence of E. coli isolated from IBD patients for diagnostic or epidemiological studies and to identify new strategies for therapeutic intervention to block the interaction between AIEC and gut mucosa in the early stages of IBD.Nicolas DreuxJérémy DenizotMargarita Martinez-MedinaAlexander MellmannMaria BilligDagmara KisielaSujay ChattopadhyayEvgeni SokurenkoChristel NeutCorinne Gower-RousseauJean-Frédéric ColombelRichard BonnetArlette Darfeuille-MichaudNicolas BarnichPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 9, Iss 1, p e1003141 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Nicolas Dreux Jérémy Denizot Margarita Martinez-Medina Alexander Mellmann Maria Billig Dagmara Kisiela Sujay Chattopadhyay Evgeni Sokurenko Christel Neut Corinne Gower-Rousseau Jean-Frédéric Colombel Richard Bonnet Arlette Darfeuille-Michaud Nicolas Barnich Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
description	Adherent-invasive Escherichia coli (AIEC) are abnormally predominant on Crohn's disease (CD) ileal mucosa. AIEC reference strain LF82 adheres to ileal enterocytes via the common type 1 pili adhesin FimH and recognizes CEACAM6 receptors abnormally expressed on CD ileal epithelial cells. The fimH genes of 45 AIEC and 47 non-AIEC strains were sequenced. The phylogenetic tree based on fimH DNA sequences indicated that AIEC strains predominantly express FimH with amino acid mutations of a recent evolutionary origin - a typical signature of pathoadaptive changes of bacterial pathogens. Point mutations in FimH, some of a unique AIEC-associated nature, confer AIEC bacteria a significantly higher ability to adhere to CEACAM-expressing T84 intestinal epithelial cells. Moreover, in the LF82 strain, the replacement of fimH(LF82) (expressing FimH with an AIEC-associated mutation) with fimH(K12) (expressing FimH of commensal E. coli K12) decreased the ability of bacteria to persist and to induce severe colitis and gut inflammation in infected CEABAC10 transgenic mice expressing human CEACAM receptors. Our results highlight a mechanism of AIEC virulence evolution that involves selection of amino acid mutations in the common bacterial traits, such as FimH protein, and leads to the development of chronic inflammatory bowel disease (IBD) in a genetically susceptible host. The analysis of fimH SNPs may be a useful method to predict the potential virulence of E. coli isolated from IBD patients for diagnostic or epidemiological studies and to identify new strategies for therapeutic intervention to block the interaction between AIEC and gut mucosa in the early stages of IBD.
format	article
author	Nicolas Dreux Jérémy Denizot Margarita Martinez-Medina Alexander Mellmann Maria Billig Dagmara Kisiela Sujay Chattopadhyay Evgeni Sokurenko Christel Neut Corinne Gower-Rousseau Jean-Frédéric Colombel Richard Bonnet Arlette Darfeuille-Michaud Nicolas Barnich
author_facet	Nicolas Dreux Jérémy Denizot Margarita Martinez-Medina Alexander Mellmann Maria Billig Dagmara Kisiela Sujay Chattopadhyay Evgeni Sokurenko Christel Neut Corinne Gower-Rousseau Jean-Frédéric Colombel Richard Bonnet Arlette Darfeuille-Michaud Nicolas Barnich
author_sort	Nicolas Dreux
title	Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
title_short	Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
title_full	Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
title_fullStr	Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
title_full_unstemmed	Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.
title_sort	point mutations in fimh adhesin of crohn's disease-associated adherent-invasive escherichia coli enhance intestinal inflammatory response.
publisher	Public Library of Science (PLoS)
publishDate	2013
url	https://doaj.org/article/e4669ff6ea7c4a89b4023b6ba16045c3
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Point mutations in FimH adhesin of Crohn's disease-associated adherent-invasive Escherichia coli enhance intestinal inflammatory response.

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