SNP-mediated binding of TBX1 to the enhancer element of IL-10 reduces the risk of Behçet's disease

Epigenomics. 2021 Oct;13(19):1523-1537. doi: 10.2217/epi-2021-0215. Epub 2021 Oct 6.

Abstract

Aims: The genetic association between Behçet's disease susceptibility and IL-10 has been confirmed in multiple cohorts, but the underlying mechanism of this association remains unclear. Materials & methods: We combined public resources and laboratory experiments (electrophoretic mobility shift assays, chromatin immunoprecipitation, luciferase reporter gene and CRISPR/Cas9 genome editing) to analyze transcription factor binding and enhancer activity controlling IL-10 expression. Results & conclusion: The T allele of noncoding rs3024490 within super-enhancer elements is able to specifically bind TBX1 and, in turn, promotes the enhancer activity and increased expression of IL-10. However, a relative deficiency in TBX1 in Behçet's disease patients leads to the low expression of IL-10 and increased risk of developing Behçet's disease.

Keywords: Behçet’s disease; IL-10; TBX1; polymorphisms; super-enhancer.

Plain language summary

Lay abstract Behçet’s disease is a prominant cause of blindness. Previous reports show that genetic factors are linked with this disease, although the exact genetic mechanism is unclear. Many of these genetic factors are involved in the control of the immune response, including a large family of proteins known as cytokines. Some of the cytokines are proinflammatory while others can dampen the inflammatory response. An example of the latter is the IL-10 cytokine. We found that individuals carrying a specific site in the noncoding region of the IL-10 gene had a higher risk of Behçet’s disease than other noncarriers. This study was designed to further investigate the biological mechanisms explaining the role of the specific site in the development of Behçet’s disease. The results show that this specific site affects the binding of an important transcription factor, TBX1, which reduces IL-10 production. The dysregulated control of IL-10 explains why individuals with this genetic trait are more susceptible to developing Behçet’s disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Behcet Syndrome / diagnosis
  • Behcet Syndrome / etiology*
  • Behcet Syndrome / metabolism*
  • Binding Sites
  • Cell Line
  • Enhancer Elements, Genetic*
  • Gene Editing
  • Gene Expression
  • Gene Knockdown Techniques
  • Genetic Association Studies
  • Genetic Predisposition to Disease
  • Humans
  • Interleukin-10 / genetics*
  • Models, Biological
  • Polymorphism, Single Nucleotide*
  • Protein Binding
  • T-Box Domain Proteins / genetics*
  • T-Box Domain Proteins / metabolism*

Substances

  • IL10 protein, human
  • T-Box Domain Proteins
  • TBX1 protein, human
  • Interleukin-10