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Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids

The life span of intestinal epithelial cells (IECs) is short (3–5 days), and its regulation is thought to be important for homeostasis of the intestinal epithelium. We have now investigated the role of commensal bacteria in regulation of IEC turnover in the small intestine. The proliferative activit...

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Autores principales: Park, Jung-ha, Kotani, Takenori, Konno, Tasuku, Setiawan, Jajar, Kitamura, Yasuaki, Imada, Shinya, Usui, Yutaro, Hatano, Naoya, Shinohara, Masakazu, Saito, Yasuyuki, Murata, Yoji, Matozaki, Takashi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4883796/
https://www.ncbi.nlm.nih.gov/pubmed/27232601
http://dx.doi.org/10.1371/journal.pone.0156334
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author Park, Jung-ha
Kotani, Takenori
Konno, Tasuku
Setiawan, Jajar
Kitamura, Yasuaki
Imada, Shinya
Usui, Yutaro
Hatano, Naoya
Shinohara, Masakazu
Saito, Yasuyuki
Murata, Yoji
Matozaki, Takashi
author_facet Park, Jung-ha
Kotani, Takenori
Konno, Tasuku
Setiawan, Jajar
Kitamura, Yasuaki
Imada, Shinya
Usui, Yutaro
Hatano, Naoya
Shinohara, Masakazu
Saito, Yasuyuki
Murata, Yoji
Matozaki, Takashi
author_sort Park, Jung-ha
collection PubMed
description The life span of intestinal epithelial cells (IECs) is short (3–5 days), and its regulation is thought to be important for homeostasis of the intestinal epithelium. We have now investigated the role of commensal bacteria in regulation of IEC turnover in the small intestine. The proliferative activity of IECs in intestinal crypts as well as the migration of these cells along the crypt-villus axis were markedly attenuated both in germ-free mice and in specific pathogen–free (SPF) mice treated with a mixture of antibiotics, with antibiotics selective for Gram-positive bacteria being most effective in this regard. Oral administration of chloroform-treated feces of SPF mice to germ-free mice resulted in a marked increase in IEC turnover, suggesting that spore-forming Gram-positive bacteria contribute to this effect. Oral administration of short-chain fatty acids (SCFAs) as bacterial fermentation products also restored the turnover of IECs in antibiotic-treated SPF mice as well as promoted the development of intestinal organoids in vitro. Antibiotic treatment reduced the phosphorylation levels of ERK, ribosomal protein S6, and STAT3 in IECs of SPF mice. Our results thus suggest that Gram-positive commensal bacteria are a major determinant of IEC turnover, and that their stimulatory effect is mediated by SCFAs.
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spelling pubmed-48837962016-06-10 Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids Park, Jung-ha Kotani, Takenori Konno, Tasuku Setiawan, Jajar Kitamura, Yasuaki Imada, Shinya Usui, Yutaro Hatano, Naoya Shinohara, Masakazu Saito, Yasuyuki Murata, Yoji Matozaki, Takashi PLoS One Research Article The life span of intestinal epithelial cells (IECs) is short (3–5 days), and its regulation is thought to be important for homeostasis of the intestinal epithelium. We have now investigated the role of commensal bacteria in regulation of IEC turnover in the small intestine. The proliferative activity of IECs in intestinal crypts as well as the migration of these cells along the crypt-villus axis were markedly attenuated both in germ-free mice and in specific pathogen–free (SPF) mice treated with a mixture of antibiotics, with antibiotics selective for Gram-positive bacteria being most effective in this regard. Oral administration of chloroform-treated feces of SPF mice to germ-free mice resulted in a marked increase in IEC turnover, suggesting that spore-forming Gram-positive bacteria contribute to this effect. Oral administration of short-chain fatty acids (SCFAs) as bacterial fermentation products also restored the turnover of IECs in antibiotic-treated SPF mice as well as promoted the development of intestinal organoids in vitro. Antibiotic treatment reduced the phosphorylation levels of ERK, ribosomal protein S6, and STAT3 in IECs of SPF mice. Our results thus suggest that Gram-positive commensal bacteria are a major determinant of IEC turnover, and that their stimulatory effect is mediated by SCFAs. Public Library of Science 2016-05-27 /pmc/articles/PMC4883796/ /pubmed/27232601 http://dx.doi.org/10.1371/journal.pone.0156334 Text en © 2016 Park et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Park, Jung-ha
Kotani, Takenori
Konno, Tasuku
Setiawan, Jajar
Kitamura, Yasuaki
Imada, Shinya
Usui, Yutaro
Hatano, Naoya
Shinohara, Masakazu
Saito, Yasuyuki
Murata, Yoji
Matozaki, Takashi
Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids
title Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids
title_full Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids
title_fullStr Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids
title_full_unstemmed Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids
title_short Promotion of Intestinal Epithelial Cell Turnover by Commensal Bacteria: Role of Short-Chain Fatty Acids
title_sort promotion of intestinal epithelial cell turnover by commensal bacteria: role of short-chain fatty acids
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4883796/
https://www.ncbi.nlm.nih.gov/pubmed/27232601
http://dx.doi.org/10.1371/journal.pone.0156334
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