Variants in TRIM22 That Affect NOD2 Signaling Are Associated With Very-Early-Onset Inflammatory Bowel Disease

Gastroenterology. 2016 May;150(5):1196-1207. doi: 10.1053/j.gastro.2016.01.031. Epub 2016 Feb 4.

Abstract

Background & aims: Severe forms of inflammatory bowel disease (IBD) that develop in very young children can be caused by variants in a single gene. We performed whole-exome sequence (WES) analysis to identify genetic factors that might cause granulomatous colitis and severe perianal disease, with recurrent bacterial and viral infections, in an infant of consanguineous parents.

Methods: We performed targeted WES analysis of DNA collected from the patient and her parents. We validated our findings by a similar analysis of DNA from 150 patients with very-early-onset IBD not associated with known genetic factors analyzed in Toronto, Oxford, and Munich. We compared gene expression signatures in inflamed vs noninflamed intestinal and rectal tissues collected from patients with treatment-resistant Crohn's disease who participated in a trial of ustekinumab. We performed functional studies of identified variants in primary cells from patients and cell culture.

Results: We identified a homozygous variant in the tripartite motif containing 22 gene (TRIM22) of the patient, as well as in 2 patients with a disease similar phenotype. Functional studies showed that the variant disrupted the ability of TRIM22 to regulate nucleotide binding oligomerization domain containing 2 (NOD2)-dependent activation of interferon-beta signaling and nuclear factor-κB. Computational studies demonstrated a correlation between the TRIM22-NOD2 network and signaling pathways and genetic factors associated very early onset and adult-onset IBD. TRIM22 is also associated with antiviral and mycobacterial effectors and markers of inflammation, such as fecal calprotectin, C-reactive protein, and Crohn's disease activity index scores.

Conclusions: In WES and targeted exome sequence analyses of an infant with severe IBD characterized by granulomatous colitis and severe perianal disease, we identified a homozygous variant of TRIM22 that affects the ability of its product to regulate NOD2. Combined computational and functional studies showed that the TRIM22-NOD2 network regulates antiviral and antibacterial signaling pathways that contribute to inflammation. Further study of this network could lead to new disease markers and therapeutic targets for patients with very early and adult-onset IBD.

Keywords: Antiviral and Antibacterial Networks; NF-kB; VEOIBD.

Publication types

  • Case Reports
  • Multicenter Study

MeSH terms

  • Age of Onset
  • Australia
  • Cells, Cultured
  • Computational Biology
  • Consanguinity
  • Crohn Disease / diagnosis
  • Crohn Disease / genetics*
  • Crohn Disease / metabolism
  • Crohn Disease / therapy
  • Databases, Genetic
  • England
  • Exome
  • Female
  • Gene Expression Profiling / methods
  • Gene Regulatory Networks
  • Genetic Association Studies
  • Genetic Predisposition to Disease
  • Genetic Variation*
  • Germany
  • Homozygote
  • Humans
  • Infant, Newborn
  • Minor Histocompatibility Antigens / genetics*
  • Minor Histocompatibility Antigens / metabolism
  • Nod2 Signaling Adaptor Protein / metabolism*
  • Ontario
  • Pedigree
  • Phenotype
  • Protein Interaction Maps
  • Repressor Proteins / genetics*
  • Repressor Proteins / metabolism
  • Severity of Illness Index
  • Signal Transduction*
  • Transfection
  • Tripartite Motif Proteins / genetics*
  • Tripartite Motif Proteins / metabolism

Substances

  • Minor Histocompatibility Antigens
  • NOD2 protein, human
  • Nod2 Signaling Adaptor Protein
  • Repressor Proteins
  • TRIM22 protein, human
  • Tripartite Motif Proteins

Supplementary concepts

  • Pediatric Crohn's disease