An ankylosing spondylitis-associated genetic variant in the IL23R-IL12RB2 intergenic region modulates enhancer activity and is associated with increased Th1-cell differentiation

Ann Rheum Dis. 2016 Dec;75(12):2150-2156. doi: 10.1136/annrheumdis-2015-208640. Epub 2016 Feb 25.

Abstract

Objectives: To explore the functional basis for the association between ankylosing spondylitis (AS) and single-nucleotide polymorphisms (SNPs) in the IL23R-IL12RB2 intergenic region.

Methods: We performed conditional analysis on genetic association data and used epigenetic data on chromatin remodelling and transcription factor (TF) binding to identify the primary AS-associated IL23R-IL12RB2 intergenic SNP. Functional effects were tested in luciferase reporter assays in HEK293T cells and allele-specific TF binding was investigated by electrophoretic mobility gel shift assays. IL23R and IL12RB2 mRNA levels in CD4+ T cells were compared between cases homozygous for the AS-risk 'A' allele and the protective 'G' allele. The proportions of interleukin (IL)-17A+ and interferon (IFN)-γ+ CD4+ T-cells were measured by fluorescence-activated cell sorting and compared between these AS-risk and protective genotypes.

Results: Conditional analysis identified rs11209032 as the probable causal SNP within a 1.14 kb putative enhancer between IL23R and IL12RB2. Reduced luciferase activity was seen for the risk allele (p<0.001) and reduced H3K4me1 methylation observed in CD4+ T-cells from 'A/A' homozygotes (p=0.02). The binding of nuclear extract to the risk allele was decreased ∼3.5-fold compared with the protective allele (p<0.001). The proportion of IFN-γ+ CD4+ T-cells was increased in 'A/A' homozygotes (p=0.004), but neither IL23R nor IL12RB2 mRNA was affected.

Conclusions: The rs11209032 SNP downstream of IL23R forms part of an enhancer, allelic variation of which may influence Th1-cell numbers. Homozygosity for the risk 'A' allele is associated with more IFN-γ-secreting (Th1) cells. Further work is necessary to explain the mechanisms for these important observations.

Keywords: Ankylosing Spondylitis; Gene Polymorphism; T Cells.

MeSH terms

  • Adult
  • Alleles
  • Cell Differentiation / genetics*
  • DNA, Intergenic
  • Female
  • Flow Cytometry
  • Genetic Association Studies
  • Genetic Variation
  • Genotype
  • HEK293 Cells
  • Humans
  • Male
  • Polymorphism, Single Nucleotide
  • Receptors, Interleukin / genetics*
  • Receptors, Interleukin-12 / genetics*
  • Spondylitis, Ankylosing / genetics*
  • Th1 Cells / physiology*

Substances

  • DNA, Intergenic
  • IL12RB2 protein, human
  • IL23R protein, human
  • Receptors, Interleukin
  • Receptors, Interleukin-12