Promotion of intestinal epithelial cell turnover by commensal bacteria: Role of short-chain fatty acids

Jung Ha Park, Takenori Kotani, Tasuku Konno, Jajar Setiawan, Yasuaki Kitamura, Shinya Imada, Yutaro Usui, Naoya Hatano, Masakazu Shinohara, Yasuyuki Saito, Yoji Murata, Takashi Matozaki

Research output: Contribution to journalArticle

43 Citations (Scopus)

Abstract

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.

Original languageEnglish
Article numbere0156334
JournalPLoS One
Volume11
Issue number5
DOIs
Publication statusPublished - May 1 2016
Externally publishedYes

Fingerprint

Volatile Fatty Acids
short chain fatty acids
Bacteria
epithelial cells
Epithelial Cells
Specific Pathogen-Free Organisms
Pathogens
bacteria
mice
Gram-Positive Bacteria
Gram-positive bacteria
antibiotics
Anti-Bacterial Agents
pathogens
oral administration
Oral Administration
Ribosomal Protein S6
Organoids
intestinal crypts
spore-forming bacteria

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Park, J. H., Kotani, T., Konno, T., Setiawan, J., Kitamura, Y., Imada, S., ... Matozaki, T. (2016). Promotion of intestinal epithelial cell turnover by commensal bacteria: Role of short-chain fatty acids. PLoS One, 11(5), [e0156334]. https://doi.org/10.1371/journal.pone.0156334

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.

In: PLoS One, Vol. 11, No. 5, e0156334, 01.05.2016.

Research output: Contribution to journalArticle

Park, JH, Kotani, T, Konno, T, Setiawan, J, Kitamura, Y, Imada, S, Usui, Y, Hatano, N, Shinohara, M, Saito, Y, Murata, Y & Matozaki, T 2016, 'Promotion of intestinal epithelial cell turnover by commensal bacteria: Role of short-chain fatty acids', PLoS One, vol. 11, no. 5, e0156334. https://doi.org/10.1371/journal.pone.0156334
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. In: PLoS One. 2016 ; Vol. 11, No. 5.
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