Functional genomics atlas of synovial fibroblasts defining rheumatoid arthritis heritability

Genome Biol. 2021 Aug 25;22(1):247. doi: 10.1186/s13059-021-02460-6.

Abstract

Background: Genome-wide association studies have reported more than 100 risk loci for rheumatoid arthritis (RA). These loci are shown to be enriched in immune cell-specific enhancers, but the analysis so far has excluded stromal cells, such as synovial fibroblasts (FLS), despite their crucial involvement in the pathogenesis of RA. Here we integrate DNA architecture, 3D chromatin interactions, DNA accessibility, and gene expression in FLS, B cells, and T cells with genetic fine mapping of RA loci.

Results: We identify putative causal variants, enhancers, genes, and cell types for 30-60% of RA loci and demonstrate that FLS account for up to 24% of RA heritability. TNF stimulation of FLS alters the organization of topologically associating domains, chromatin state, and the expression of putative causal genes such as TNFAIP3 and IFNAR1. Several putative causal genes constitute RA-relevant functional networks in FLS with roles in cellular proliferation and activation. Finally, we demonstrate that risk variants can have joint-specific effects on target gene expression in RA FLS, which may contribute to the development of the characteristic pattern of joint involvement in RA.

Conclusion: Overall, our research provides the first direct evidence for a causal role of FLS in the genetic susceptibility for RA accounting for up to a quarter of RA heritability.

Keywords: Fibroblast-like synoviocytes; Functional genomics; Rheumatoid arthritis; Stromal cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Arthritis, Rheumatoid / genetics*
  • Arthritis, Rheumatoid / pathology*
  • Base Sequence
  • Chromatin / metabolism
  • Databases, Genetic
  • Enhancer Elements, Genetic / genetics
  • Epigenesis, Genetic / drug effects
  • Female
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibroblasts / pathology*
  • Gene Regulatory Networks / drug effects
  • Genetic Predisposition to Disease
  • Genomics*
  • Humans
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein / genetics
  • Inheritance Patterns / genetics*
  • Male
  • Middle Aged
  • Polymorphism, Single Nucleotide / genetics
  • Probability
  • Receptor, Interferon alpha-beta / metabolism
  • Receptors, Interferon / metabolism
  • Reproducibility of Results
  • Risk Factors
  • Synovial Membrane / pathology*
  • Tumor Necrosis Factor alpha-Induced Protein 3 / metabolism
  • Tumor Necrosis Factor-alpha / pharmacology
  • Young Adult

Substances

  • Chromatin
  • IFNAR1 protein, human
  • IFNGR2 protein, human
  • Immunoglobulin J Recombination Signal Sequence-Binding Protein
  • RBPJ protein, human
  • Receptors, Interferon
  • Tumor Necrosis Factor-alpha
  • Receptor, Interferon alpha-beta
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3