Collagenous Colitis Is Associated With HLA Signature and Shares Genetic Risks With Other Immune-Mediated Diseases

Gastroenterology. 2020 Aug;159(2):549-561.e8. doi: 10.1053/j.gastro.2020.04.063. Epub 2020 May 1.

Abstract

Background & aims: Collagenous colitis (CC) is an inflammatory bowel disorder with unknown etiopathogenesis involving HLA-related immune-mediated responses and environmental and genetic risk factors. We carried out an array-based genetic association study in a cohort of patients with CC and investigated the common genetic basis between CC and Crohn's disease (CD), ulcerative colitis (UC), and celiac disease.

Methods: DNA from 804 CC formalin-fixed, paraffin-embedded tissue samples was genotyped with Illumina Immunochip. Matching genotype data on control samples and CD, UC, and celiac disease cases were provided by the respective consortia. A discovery association study followed by meta-analysis with an independent cohort, polygenic risk score calculation, and cross-phenotype analyses were performed. Enrichment of regulatory expression quantitative trait loci among the CC variants was assessed in hemopoietic and intestinal cells.

Results: Three HLA alleles (HLA-B∗08:01, HLA-DRB1∗03:01, and HLA-DQB1∗02:01), related to the ancestral haplotype 8.1, were significantly associated with increased CC risk. We also identified an independent protective effect of HLA-DRB1∗04:01 on CC risk. Polygenic risk score quantifying the risk across multiple susceptibility loci was strongly associated with CC risk. An enrichment of expression quantitative trait loci was detected among the CC-susceptibility variants in various cell types. The cross-phenotype analysis identified a complex pattern of polygenic pleiotropy between CC and other immune-mediated diseases.

Conclusions: In this largest genetic study of CC to date with histologically confirmed diagnosis, we strongly implicated the HLA locus and proposed potential non-HLA mechanisms in disease pathogenesis. We also detected a shared genetic risk between CC, celiac disease, CD, and UC, which supports clinical observations of comorbidity.

Keywords: Collagenous Colitis; Crohn’s Disease; HLA; Immunochip.

Publication types

  • Multicenter Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Alleles
  • Case-Control Studies
  • Celiac Disease / genetics
  • Celiac Disease / immunology
  • Celiac Disease / pathology
  • Cohort Studies
  • Colitis, Collagenous / genetics*
  • Colitis, Collagenous / immunology
  • Colitis, Collagenous / pathology
  • Colitis, Ulcerative / genetics
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / pathology
  • Colon / pathology
  • Crohn Disease / genetics
  • Crohn Disease / immunology
  • Crohn Disease / pathology
  • Datasets as Topic
  • Genetic Association Studies
  • Genetic Predisposition to Disease*
  • HLA Antigens / genetics*
  • HLA Antigens / immunology
  • Humans
  • Multifactorial Inheritance / immunology
  • Polymorphism, Single Nucleotide
  • Quantitative Trait Loci
  • Risk Factors
  • Tissue Array Analysis

Substances

  • HLA Antigens