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High cellulose diet promotes intestinal motility through regulating intestinal immune homeostasis and serotonin biosynthesis

  • Tao Xie , Fa Jin , Xiaokun Jia , Hengxu Mao , Yuting Xu and Shizhong Zhang ORCID logo EMAIL logo
Published/Copyright: September 18, 2021
Biological Chemistry
From the journal Biological Chemistry Volume 403 Issue 3

Abstract

It is widely accepted dietary fiber intimately linked to inflammatory and nervous diseases, which often been described with altered gastrointestinal (GI) motility. However, how dose dietary fiber modulate inflammation and crosstalk influence GI function has not been explained in detail. We found fiber-free diet reduced intestinal motility, accompanied by upregulated proinflammatory immunocytes and inflammatory cytokines in colon of mice. We also discovered high-cellulose diet increased synthesis of serotonin and expression of neurotrophic factors, both of that have been reported involved in promoting intestinal motility. In addition, metabolomics analysis showed increased tryptophan metabolites in high-cellulose diet mice, which happened to be required for serotonin biosynthesis. Further analysis revealed high-cellulose diet changed the composition of gut microbiota, in particular by altering the ratio of Firmicutes to Bacteroidetes, consequently, concentration of short-chain fatty acids (SCFAs), especially acetate. Orally administration of acetate confirmed its modulating to serotonin synthesis, neurotrophic factors expression and immunocyte differentiation through regulating histone deacetylase (HDAC3) activity in colon. Together, our results demonstrated high-cellulose diet promote intestinal motility through regulating intestinal homeostasis and enteric nervous system by increasing acetate production and HDAC3 inhibition. Thus, rich cellulose diet or acetate supplement can be considered as dietary advice to improve clinically intestinal motility insufficiency.

Keywords: acetate; gut microbiota; high cellulose diet; histone deacetylase; intestinal motility
Corresponding author: Shizhong Zhang, Department of Neurosurgery, Zhujiang Hospital, Southern Medical University, The National Key Clinical Specialty, The Engineering Technology Research Center of Education Ministry of China, Guangdong Provincial Key Laboratory on Brain Function Repair and Regeneration, The Neurosurgery Institute of Guangdong Province, Guangzhou 510282, China, E-mail:

Funding source: Guangdong Science and Technology Plan Foundation http://pro.gdstc.gd.gov.cn/egrantweb/index###

Award Identifier / Grant number: 2017A020215044

Acknowledgments

We thank members of our group for insightful discussion during the course of this study.

  1. Author contributions: Tao Xie conceived and designed the experiments; Fa Jin and Xiaokun Jia performed the experiments; Hengxu Mao and Yuting Xu analyzed the data; Tao Xie and Shizhong Zhang wrote the paper. All authors read and approved the final manuscript.

  2. Research funding: This work was supported by grants from the Guangdong Science and Technology Plan Foundation (2017A020215044 to Tao Xie, DOI: http://pro.gdstc.gd.gov.cn/egrantweb/index###). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

  3. Availability of data and material: The data used to support the findings of this study are available from the corresponding author upon request.

  4. Ethics approval: All animal protocols and procedures were conducted under the approval of the Ethical Committee of Guangdong Provincial Animal Experiment Center. All animals received human care and that study protocols comply with the institution’s guidelines.

  5. Conflict of interest statement: The authors declare that they have no competing interests.

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Received: 2021-04-02
Accepted: 2021-09-07
Published Online: 2021-09-18
Published in Print: 2022-02-23

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Articles in the same Issue

  1. Frontmatter
  2. Research Articles
  3. Inhibitory effect of mitoquinone against the α-synuclein fibrillation and relevant neurotoxicity: possible role in inhibition of Parkinson’s disease
  4. Effect of myeloperoxidase oxidation and N-homocysteinylation of high-density lipoprotein on endothelial repair function
  5. High cellulose diet promotes intestinal motility through regulating intestinal immune homeostasis and serotonin biosynthesis
  6. Quercetin increases mitochondrial proteins (VDAC and SDH) and downmodulates AXL and PIM-1 tyrosine kinase receptors in NRAS melanoma cells
  7. Regulation of transforming growth factor-β1-stimulation of Runx2 acetylation for matrix metalloproteinase 13 expression in osteoblastic cells
  8. M6A methylation-mediated elevation of SM22α inhibits the proliferation and migration of vascular smooth muscle cells and ameliorates intimal hyperplasia in type 2 diabetes mellitus
  9. Characterization of hepatic zonation in mice by mass-spectrometric and antibody-based proteomics approaches
  10. Characterization of a fluorescent 1,8-naphthalimide-functionalized PAMAM dendrimer and its Cu(ii) complexes as cytotoxic drugs: EPR and biological studies in myeloid tumor cells
https://doi.org/10.1515/hsz-2021-0216
Keywords for this article
acetate; gut microbiota; high cellulose diet; histone deacetylase; intestinal motility

Articles in the same Issue

  1. Frontmatter
  2. Research Articles
  3. Inhibitory effect of mitoquinone against the α-synuclein fibrillation and relevant neurotoxicity: possible role in inhibition of Parkinson’s disease
  4. Effect of myeloperoxidase oxidation and N-homocysteinylation of high-density lipoprotein on endothelial repair function
  5. High cellulose diet promotes intestinal motility through regulating intestinal immune homeostasis and serotonin biosynthesis
  6. Quercetin increases mitochondrial proteins (VDAC and SDH) and downmodulates AXL and PIM-1 tyrosine kinase receptors in NRAS melanoma cells
  7. Regulation of transforming growth factor-β1-stimulation of Runx2 acetylation for matrix metalloproteinase 13 expression in osteoblastic cells
  8. M6A methylation-mediated elevation of SM22α inhibits the proliferation and migration of vascular smooth muscle cells and ameliorates intimal hyperplasia in type 2 diabetes mellitus
  9. Characterization of hepatic zonation in mice by mass-spectrometric and antibody-based proteomics approaches
  10. Characterization of a fluorescent 1,8-naphthalimide-functionalized PAMAM dendrimer and its Cu(ii) complexes as cytotoxic drugs: EPR and biological studies in myeloid tumor cells
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