l-Theanine Alleviates Ulcerative Colitis by Regulating Colon Immunity via the Gut Microbiota in an MHC-II-Dependent Manner

J Agric Food Chem. 2024 Sep 11;72(36):19852-19868. doi: 10.1021/acs.jafc.4c04379. Epub 2024 Aug 28.

Abstract

Alterations to the gut microbiota are associated with ulcerative colitis (UC), whereas restoration of normobiosis can effectively alleviate UC. l-Theanine has been shown to reshape the gut microbiota and regulate gut immunity. To investigate the mechanisms by which l-theanine alleviates UC, we used l-theanine and l-theanine fecal microbiota solution to treat UC mice. In this study, we used l-theanine and l-theanine fecal microbiota solution to treat UC mice to explore the mechanism by which l-theanine alleviates UC. By reducing inflammation in the colon, we demonstrated that l-theanine alleviates symptoms of UC. Meanwhile, l-theanine can improve the abundance of microbiota related to short-chain fatty acid, bile acid, and tryptophan production. Single-cell sequencing results indicated that l-theanine-mediated suppression of UC was associated with immune cell changes, especially regarding macrophages and T and B cells, and validated the immune cell responses to the gut microbiota. Further, flow cytometry results showed that the ability of dendritic cells, macrophages, and monocytes to present microbiota antigens to colonic T cells in an MHC-II-dependent manner was reduced after treating normal mouse fecal donors with l-theanine. These results demonstrate that l-theanine modulates colon adaptive and innate immunity by regulating the gut microbiota in an MHC-II-dependent manner, thereby alleviating UC.

Keywords: colon immunity; fecal microbiota transplantation; gut microbiota; l-theanine; single-cell sequencing; ulcerative colitis.

MeSH terms

  • Animals
  • Bacteria / classification
  • Bacteria / drug effects
  • Bacteria / genetics
  • Bacteria / immunology
  • Bacteria / isolation & purification
  • Colitis, Ulcerative* / drug therapy
  • Colitis, Ulcerative* / immunology
  • Colitis, Ulcerative* / microbiology
  • Colon* / drug effects
  • Colon* / immunology
  • Colon* / microbiology
  • Feces / microbiology
  • Gastrointestinal Microbiome* / drug effects
  • Glutamates* / administration & dosage
  • Glutamates* / pharmacology
  • Histocompatibility Antigens Class II / genetics
  • Histocompatibility Antigens Class II / immunology
  • Humans
  • Macrophages / drug effects
  • Macrophages / immunology
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology

Substances

  • theanine
  • Glutamates
  • Histocompatibility Antigens Class II