Translocation of Viable Gut Microbiota to Mesenteric Adipose Drives Formation of Creeping Fat in Humans

Cell. 2020 Oct 29;183(3):666-683.e17. doi: 10.1016/j.cell.2020.09.009. Epub 2020 Sep 28.

Abstract

A mysterious feature of Crohn's disease (CD) is the extra-intestinal manifestation of "creeping fat" (CrF), defined as expansion of mesenteric adipose tissue around the inflamed and fibrotic intestine. In the current study, we explore whether microbial translocation in CD serves as a central cue for CrF development. We discovered a subset of mucosal-associated gut bacteria that consistently translocated and remained viable in CrF in CD ileal surgical resections, and identified Clostridium innocuum as a signature of this consortium with strain variation between mucosal and adipose isolates, suggesting preference for lipid-rich environments. Single-cell RNA sequencing characterized CrF as both pro-fibrotic and pro-adipogenic with a rich milieu of activated immune cells responding to microbial stimuli, which we confirm in gnotobiotic mice colonized with C. innocuum. Ex vivo validation of expression patterns suggests C. innocuum stimulates tissue remodeling via M2 macrophages, leading to an adipose tissue barrier that serves to prevent systemic dissemination of bacteria.

Keywords: Crohn’s disease; adipogenesis; creeping fat; fibrosis; human microbiome; ileum; inflammatory bowel diseases; macrophages; mesenteric adipose; translocation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / microbiology*
  • Adipose Tissue / pathology
  • Animals
  • Bacterial Translocation*
  • Biodiversity
  • Biomarkers / metabolism
  • Cell Polarity
  • Cells, Cultured
  • Colitis, Ulcerative / pathology
  • Crohn Disease / microbiology
  • Crohn Disease / pathology
  • Gastrointestinal Microbiome* / genetics
  • Gene Expression Regulation
  • Germ-Free Life
  • Humans
  • Ileum / microbiology
  • Ileum / pathology
  • Lipopolysaccharides / metabolism
  • Macrophages / metabolism
  • Mesentery / microbiology*
  • Metagenome
  • Metagenomics
  • Mice
  • Mice, Inbred C57BL
  • Phenotype
  • RNA, Ribosomal, 16S / genetics
  • Stem Cells / metabolism

Substances

  • Biomarkers
  • Lipopolysaccharides
  • RNA, Ribosomal, 16S