Dietary cellulose prevents gut inflammation by modulating lipid metabolism and gut microbiota

Gut Microbes. 2020 Jul 3;11(4):944-961. doi: 10.1080/19490976.2020.1730149. Epub 2020 Mar 5.

Abstract

A Western diet comprising high fat, high carbohydrate, and low fiber content has been suggested to contribute to an increased prevalence of colitis. To clarify the effect of dietary cellulose (an insoluble fiber) on gut homeostasis, for 3 months mice were fed a high-cellulose diet (HCD) or a low-cellulose diet (LCD) based on the AIN-93G formulation. Histologic evaluation showed crypt atrophy and goblet cell depletion in the colons of LCD-fed mice. RNA-sequencing analysis showed a higher expression of genes associated with immune system processes, especially those of chemokines and their receptors, in the colon tissues of LCD-fed mice than in those of HCD-fed mice. The HCD was protective against dextran sodium sulfate-induced colitis in mice, while LCD exacerbated gut inflammation; however, the depletion of gut microbiota by antibiotic treatment diminished both beneficial and non-beneficial effects of the HCD and LCD on colitis, respectively. A comparative analysis of the cecal contents of mice fed the HCD or the LCD showed that the LCD did not influence the diversity of gut microbiota, but it resulted in a higher and lower abundance of Oscillibacter and Akkermansia organisms, respectively. Additionally, linoleic acid, nicotinate, and nicotinamide pathways were most affected by cellulose intake, while the levels of short-chain fatty acids were comparable in HCD- and LCD-fed mice. Finally, oral administration of Akkermansia muciniphila to LCD-fed mice elevated crypt length, increased goblet cells, and ameliorated colitis. These results suggest that dietary cellulose plays a beneficial role in maintaining gut homeostasis through the alteration of gut microbiota and metabolites.

Keywords: Akkermansia; Cellulose; colitis; dextran sulfate sodium; insoluble fiber; microbiota.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Akkermansia / physiology
  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Bacteria / growth & development*
  • Cecum / microbiology
  • Cellulose / administration & dosage*
  • Colitis / prevention & control*
  • Colon / metabolism
  • Diet
  • Diet, Carbohydrate-Restricted
  • Dietary Carbohydrates / administration & dosage*
  • Female
  • Gastrointestinal Microbiome*
  • Homeostasis
  • Inflammation / genetics
  • Lipid Metabolism*
  • Metabolome
  • Mice
  • Mice, Inbred C57BL
  • RNA-Seq
  • Up-Regulation

Substances

  • Anti-Bacterial Agents
  • Dietary Carbohydrates
  • Cellulose

Supplementary concepts

  • Akkermansia muciniphila

Grants and funding

This work was supported by the National Research Foundation of Korea [NRF-2017R1A2B3002132, NRF-2019M3C9A6082556 and NRF-2019M3C9A6082487] and by Basic Science Research Program through the National Research Foundation of Korea funded by the Ministry of Education (NRF-2019R1A6A3A01091268 to Y. K.).