The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection

ABSTRACT The intestinal tract is the largest reservoir of microbes in the human body. The intestinal microbiota is thought to be able to modulate alterations of the gut induced by enteropathogens, thereby maintaining homeostasis. Listeria monocytogenes is the agent of listeriosis, an infection trans...

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Autores principales:	Cristel Archambaud, Odile Sismeiro, Joern Toedling, Guillaume Soubigou, Christophe Bécavin, Pierre Lechat, Alice Lebreton, Constance Ciaudo, Pascale Cossart
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8ab4d02e3d9046a5953c5a922454b74b
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spelling	oai:doaj.org-article:8ab4d02e3d9046a5953c5a922454b74b2021-11-15T15:42:32ZThe Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection10.1128/mBio.00707-132150-7511https://doaj.org/article/8ab4d02e3d9046a5953c5a922454b74b2013-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00707-13https://doaj.org/toc/2150-7511ABSTRACT The intestinal tract is the largest reservoir of microbes in the human body. The intestinal microbiota is thought to be able to modulate alterations of the gut induced by enteropathogens, thereby maintaining homeostasis. Listeria monocytogenes is the agent of listeriosis, an infection transmitted to humans upon ingestion of contaminated food. Crossing of the intestinal barrier is a critical step of the infection before dissemination into deeper organs. Here, we investigated the role of the intestinal microbiota in the regulation of host protein-coding genes and microRNA (miRNA or miR) expression during Listeria infection. We first established the intestinal miRNA signatures corresponding to the 10 most highly expressed miRNAs in the murine ileum of conventional and germfree mice, noninfected and infected with Listeria. Next, we identified 6 miRNAs whose expression decreased upon Listeria infection in conventional mice. Strikingly, five of these miRNA expression variations (in miR-143, miR-148a, miR-200b, miR-200c, and miR-378) were dependent on the presence of the microbiota. In addition, as is already known, protein-coding genes were highly affected by infection in both conventional and germfree mice. By crossing bioinformatically the predicted targets of the miRNAs to our whole-genome transcriptomic data, we revealed an miRNA-mRNA network that suggested miRNA-mediated global regulation during intestinal infection. Other recent studies have revealed an miRNA response to either bacterial pathogens or commensal bacteria. In contrast, our work provides an unprecedented insight into the impact of the intestinal microbiota on host transcriptional reprogramming during infection by a human pathogen. IMPORTANCE While the crucial role of miRNAs in regulating the host response to bacterial infection is increasingly recognized, the involvement of the intestinal microbiota in the regulation of miRNA expression has not been explored in detail. Here, we investigated the impact of the intestinal microbiota on the regulation of protein-coding genes and miRNA expression in a host infected by L. monocytogenes, a food-borne pathogen. We show that the microbiota interferes with the microRNA response upon oral Listeria infection and identify several protein-coding target genes whose expression correlates inversely with that of the miRNA. Further investigations of the regulatory networks involving miR-143, miR-148a, miR-200b, miR-200c, and miR-378 will provide new insights into the impact of the intestinal microbiota on the host upon bacterial infection.Cristel ArchambaudOdile SismeiroJoern ToedlingGuillaume SoubigouChristophe BécavinPierre LechatAlice LebretonConstance CiaudoPascale CossartAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 6 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Cristel Archambaud Odile Sismeiro Joern Toedling Guillaume Soubigou Christophe Bécavin Pierre Lechat Alice Lebreton Constance Ciaudo Pascale Cossart The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection
description	ABSTRACT The intestinal tract is the largest reservoir of microbes in the human body. The intestinal microbiota is thought to be able to modulate alterations of the gut induced by enteropathogens, thereby maintaining homeostasis. Listeria monocytogenes is the agent of listeriosis, an infection transmitted to humans upon ingestion of contaminated food. Crossing of the intestinal barrier is a critical step of the infection before dissemination into deeper organs. Here, we investigated the role of the intestinal microbiota in the regulation of host protein-coding genes and microRNA (miRNA or miR) expression during Listeria infection. We first established the intestinal miRNA signatures corresponding to the 10 most highly expressed miRNAs in the murine ileum of conventional and germfree mice, noninfected and infected with Listeria. Next, we identified 6 miRNAs whose expression decreased upon Listeria infection in conventional mice. Strikingly, five of these miRNA expression variations (in miR-143, miR-148a, miR-200b, miR-200c, and miR-378) were dependent on the presence of the microbiota. In addition, as is already known, protein-coding genes were highly affected by infection in both conventional and germfree mice. By crossing bioinformatically the predicted targets of the miRNAs to our whole-genome transcriptomic data, we revealed an miRNA-mRNA network that suggested miRNA-mediated global regulation during intestinal infection. Other recent studies have revealed an miRNA response to either bacterial pathogens or commensal bacteria. In contrast, our work provides an unprecedented insight into the impact of the intestinal microbiota on host transcriptional reprogramming during infection by a human pathogen. IMPORTANCE While the crucial role of miRNAs in regulating the host response to bacterial infection is increasingly recognized, the involvement of the intestinal microbiota in the regulation of miRNA expression has not been explored in detail. Here, we investigated the impact of the intestinal microbiota on the regulation of protein-coding genes and miRNA expression in a host infected by L. monocytogenes, a food-borne pathogen. We show that the microbiota interferes with the microRNA response upon oral Listeria infection and identify several protein-coding target genes whose expression correlates inversely with that of the miRNA. Further investigations of the regulatory networks involving miR-143, miR-148a, miR-200b, miR-200c, and miR-378 will provide new insights into the impact of the intestinal microbiota on the host upon bacterial infection.
format	article
author	Cristel Archambaud Odile Sismeiro Joern Toedling Guillaume Soubigou Christophe Bécavin Pierre Lechat Alice Lebreton Constance Ciaudo Pascale Cossart
author_facet	Cristel Archambaud Odile Sismeiro Joern Toedling Guillaume Soubigou Christophe Bécavin Pierre Lechat Alice Lebreton Constance Ciaudo Pascale Cossart
author_sort	Cristel Archambaud
title	The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection
title_short	The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection
title_full	The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection
title_fullStr	The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection
title_full_unstemmed	The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection
title_sort	intestinal microbiota interferes with the microrna response upon oral <italic toggle="yes">listeria</italic> infection
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/8ab4d02e3d9046a5953c5a922454b74b
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The Intestinal Microbiota Interferes with the microRNA Response upon Oral <italic toggle="yes">Listeria</italic> Infection

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