Somatic Evolution in Non-neoplastic IBD-Affected Colon

Cell. 2020 Aug 6;182(3):672-684.e11. doi: 10.1016/j.cell.2020.06.036. Epub 2020 Jul 21.

Abstract

Inflammatory bowel disease (IBD) is a chronic inflammatory disease associated with increased risk of gastrointestinal cancers. We whole-genome sequenced 446 colonic crypts from 46 IBD patients and compared these to 412 crypts from 41 non-IBD controls from our previous publication on the mutation landscape of the normal colon. The average mutation rate of affected colonic epithelial cells is 2.4-fold that of healthy colon, and this increase is mostly driven by acceleration of mutational processes ubiquitously observed in normal colon. In contrast to the normal colon, where clonal expansions outside the confines of the crypt are rare, we observed widespread millimeter-scale clonal expansions. We discovered non-synonymous mutations in ARID1A, FBXW7, PIGR, ZC3H12A, and genes in the interleukin 17 and Toll-like receptor pathways, under positive selection in IBD. These results suggest distinct selection mechanisms in the colitis-affected colon and that somatic mutations potentially play a causal role in IBD pathogenesis.

Keywords: Crohn's disease; IL17; PIGR; ZC3H12A; inflammatory bowel disease; intestinal epithelia; mutation rate; mutational signatures; somatic mutations; ulcerative colitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Aging / genetics
  • Clonal Evolution / genetics*
  • Clonal Evolution / immunology
  • Colitis / genetics*
  • Colitis / metabolism
  • Colitis, Ulcerative / genetics
  • Colitis, Ulcerative / metabolism
  • Crohn Disease / genetics
  • Crohn Disease / metabolism
  • DNA-Binding Proteins / genetics
  • Epithelial Cells / metabolism
  • Epithelial Cells / pathology
  • F-Box-WD Repeat-Containing Protein 7 / genetics
  • Female
  • Humans
  • INDEL Mutation
  • Inflammatory Bowel Diseases / genetics*
  • Inflammatory Bowel Diseases / immunology
  • Inflammatory Bowel Diseases / metabolism
  • Inflammatory Bowel Diseases / pathology
  • Interleukin-17 / metabolism
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Male
  • Middle Aged
  • Mutation Rate*
  • Phylogeny
  • Point Mutation
  • Receptors, Cell Surface / genetics
  • Ribonucleases / genetics
  • Toll-Like Receptors / genetics
  • Transcription Factors / genetics
  • Whole Genome Sequencing

Substances

  • ARID1A protein, human
  • DNA-Binding Proteins
  • F-Box-WD Repeat-Containing Protein 7
  • FBXW7 protein, human
  • Interleukin-17
  • OSCAR protein, human
  • Receptors, Cell Surface
  • Toll-Like Receptors
  • Transcription Factors
  • Ribonucleases
  • ZC3H12A protein, human