Promotion of Inflammatory Arthritis by Interferon Regulatory Factor 5 in a Mouse Model

Arthritis Rheumatol. 2015 Dec;67(12):3146-57. doi: 10.1002/art.39321.

Abstract

Objective: Polymorphisms in the transcription factor interferon regulatory factor 5 (IRF5) are associated with an increased risk of developing rheumatoid arthritis (RA). This study was undertaken to determine the role of IRF5 in a mouse model of arthritis development.

Methods: K/BxN serum-transfer arthritis was induced in mice deficient in IRF5, or lacking IRF5 only in myeloid cells, and arthritis severity was evaluated. K/BxN arthritis was also induced in mice deficient in TRIF, Toll-like receptor 2 (TLR2), TLR3, TLR4, and TLR7 to determine the pathways through which IRF5 might promote arthritis. In vitro studies were performed to determine the role of IRF5 in interleukin-1 (IL-1) receptor and TLR signaling.

Results: Arthritis severity was reduced in IRF5-deficient, TRIF-deficient, TLR3-deficient, and TLR7-deficient mice. The expression of multiple genes regulating neutrophil recruitment or function and bioactive IL-1β formation was reduced in the joints during active arthritis in IRF5-deficient mice. In vitro studies showed that TLR7 and the TRIF-dependent TLR3 pathway induce proinflammatory cytokine production in disease-relevant cell types in an IRF5-dependent manner.

Conclusion: Our findings indicate that IRF5 contributes to disease pathogenesis in inflammatory arthritis. This is likely due at least in part to the role of IRF5 in mediating proinflammatory cytokine production downstream of TLR7 and TLR3. Since TLR7 and TLR3 are both RNA-sensing TLRs, this suggests that endogenous RNA ligands present in the inflamed joint promote arthritis development. These findings may be relevant to human RA, since RNA capable of activating TLR7 and TLR3 is present in synovial fluid and TLR7 and TLR3 are up-regulated in the joints of RA patients.

Publication types

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

MeSH terms

  • Adaptor Proteins, Vesicular Transport / genetics*
  • Adaptor Proteins, Vesicular Transport / immunology
  • Animals
  • Arthritis, Experimental / genetics*
  • Arthritis, Experimental / immunology
  • Arthritis, Rheumatoid / genetics*
  • Arthritis, Rheumatoid / immunology
  • Disease Models, Animal
  • Gene Knockdown Techniques
  • In Vitro Techniques
  • Interferon Regulatory Factors / genetics*
  • Interferon Regulatory Factors / immunology
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology
  • Membrane Glycoproteins / genetics*
  • Membrane Glycoproteins / immunology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid Cells / metabolism*
  • Receptors, Interleukin-1 / genetics
  • Receptors, Interleukin-1 / immunology
  • Severity of Illness Index
  • Signal Transduction
  • Synovial Fluid / immunology
  • Synovial Fluid / metabolism
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 3 / genetics*
  • Toll-Like Receptor 3 / immunology
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology
  • Toll-Like Receptor 7 / genetics*
  • Toll-Like Receptor 7 / immunology

Substances

  • Adaptor Proteins, Vesicular Transport
  • IL1B protein, mouse
  • Interferon Regulatory Factors
  • Interleukin-1beta
  • Irf5 protein, mouse
  • Membrane Glycoproteins
  • Receptors, Interleukin-1
  • TICAM-1 protein, mouse
  • TLR3 protein, mouse
  • Tlr2 protein, mouse
  • Tlr4 protein, mouse
  • Tlr7 protein, mouse
  • Toll-Like Receptor 2
  • Toll-Like Receptor 3
  • Toll-Like Receptor 4
  • Toll-Like Receptor 7