A Pilot Integrative Analysis of Colonic Gene Expression, Gut Microbiota, and Immune Infiltration in Primary Sclerosing Cholangitis-Inflammatory Bowel Disease: Association of Disease With Bile Acid Pathways

J Crohns Colitis. 2020 Jul 30;14(7):935-947. doi: 10.1093/ecco-jcc/jjaa021.

Abstract

Background: Although a majority of patients with PSC have colitis [PSC-IBD; primary sclerosing cholangitis-inflammatory bowel disease], this is phenotypically different from ulcerative colitis [UC]. We sought to define further the pathophysiological differences between PSC-IBD and UC, by applying a comparative and integrative approach to colonic gene expression, gut microbiota and immune infiltration data.

Methods: Colonic biopsies were collected from patients with PSC-IBD [n = 10], UC [n = 10], and healthy controls [HC; n = 10]. Shotgun RNA-sequencing for differentially expressed colonic mucosal genes [DEGs], 16S rRNA analysis for microbial profiling, and immunophenotyping were performed followed by multi-omic integration.

Results: The colonic transcriptome differed significantly between groups [p = 0.01]. Colonic transcriptomes from HC were different from both UC [1343 DEGs] and PSC-IBD [4312 DEGs]. Of these genes, only 939 had shared differential gene expression in both UC and PSC-IBD compared with HC. Imputed pathways were predominantly associated with upregulation of immune response and microbial defense in both disease cohorts compared with HC. There were 1692 DEGs between PSC-IBD and UC. Bile acid signalling pathways were upregulated in PSC-IBD compared with UC [p = 0.02]. Microbiota profiles were different between the three groups [p = 0.01]; with inferred function in PSC-IBD also being consistent with dysregulation of bile acid metabolism. Th17 cells and IL17-producing CD4 cells were increased in both PSC-IBD and UC when compared with HC [p < 0.05]. Multi-omic integration revealed networks involved in bile acid homeostasis and cancer regulation in PSC-IBD.

Conclusions: Colonic transcriptomic and microbiota analysis in PSC-IBD point toward dysregulation of colonic bile acid homeostasis compared with UC. This highlights important mechanisms and suggests the possibility of novel approaches in treating PSC-IBD.

Keywords: Autoimmune liver disease; bioinformatics; colitis; dysbiosis.

MeSH terms

  • Adult
  • Bile Acids and Salts / metabolism*
  • Case-Control Studies
  • Cholangitis, Sclerosing / etiology*
  • Cholangitis, Sclerosing / pathology
  • Colitis, Ulcerative / etiology*
  • Colitis, Ulcerative / pathology
  • Colon / pathology
  • Computational Biology
  • Female
  • Gastrointestinal Microbiome*
  • Homeostasis
  • Humans
  • Immunity / genetics
  • Immunophenotyping
  • Interleukin-17 / metabolism
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Male
  • Middle Aged
  • RNA, Ribosomal, 16S / analysis
  • Sequence Analysis, RNA
  • Signal Transduction / genetics
  • Th17 Cells / metabolism
  • Transcriptome*
  • Up-Regulation

Substances

  • Bile Acids and Salts
  • Interleukin-17
  • RNA, Ribosomal, 16S