Faecalibacterium prausnitzii inhibits interleukin-17 to ameliorate colorectal colitis in rats

PLoS One. 2014 Oct 2;9(10):e109146. doi: 10.1371/journal.pone.0109146. eCollection 2014.

Abstract

Background and aims: It has been shown that Faecalibacterium prausnitzii (F. prausnitzii), one of the dominant intestinal bacterial flora, may protect colonic mucosa against the development of inflammation and subsequent inflammatory bowel disease (IBD), with the underlying mechanisms being unclear.

Methods: The impacts of F. prausnitzii and its metabolites on IL-23/Th17/IL-17 pathway markers were determined in human monocytes and a rat model of colitis induced by 2,4,6-trinitrobenzene sulfonic acid. F. prausnitzii and its culture medium (containing complete metabolites) were used to treat the rats in vivo, as well as rat splenocytes and human monocytes in vitro. Inflammatory cytokines were measured in colon tissue, plasma and cell culture medium.

Results: The culture supernatant of F. prausnitzii increased plasma anti-Th17 cytokines (IL-10 and IL-12)and suppressed IL-17 levels in both plasma and colonic mucosa, with ameliorated colonic colitis lesions. This inhibition of IL-17 release has also been observed in both rat splenocytes and human venous monocytes in vitro. The culture supernatant of F. prausnitzii also suppressed Th17 cell differentiation induced by cytokines (TGF-ß and IL-6) and bone marrow-derived dendritic cells (BMDCs) in vitro. The metabolites of F. prausnitzii in the culture supernatant exert a stronger anti-inflammatory effect than the bacterium itself. F. prausnitzii protected the colon mucosa against the development of IBD by its metabolites, suggesting a promising potential for the use of F. prausnitzii and its metabolic products in the treatment of IBD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Body Weight
  • Cell Differentiation
  • Clostridiales / physiology*
  • Colitis / metabolism
  • Colitis / prevention & control*
  • Colon / metabolism
  • Colon / pathology
  • Disease Models, Animal
  • Fatty Acids / metabolism
  • Humans
  • In Vitro Techniques
  • Interleukin-17 / antagonists & inhibitors*
  • Rats
  • Rats, Sprague-Dawley
  • Rectum / metabolism
  • Rectum / pathology
  • Th17 Cells / cytology

Substances

  • Fatty Acids
  • Interleukin-17

Grants and funding

This study has been supported by a research grant from National Natural Science Foundation of China (No. 81170359). The authors thank the Research Center of Sine Pharmaceutical (Shanghai Sine Pharmaceutical Co., Ltd., Shanghai, China) for the generous gift of Bifidobacterium longum, and the advice provided by Ms Hongjing Yu and Mr Lichuan Guo. The authors thank Professor Changhong Liu for the technique assistance. The authors thank Dr Shaun Sandow (Physiology, University of New South Wales) for his assistance English and grammar. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.