Role of JAK-STAT signaling in the pathogenic behavior of fibroblast-like synoviocytes in rheumatoid arthritis: Effect of the novel JAK inhibitor peficitinib

Eur J Pharmacol. 2020 Sep 5:882:173238. doi: 10.1016/j.ejphar.2020.173238. Epub 2020 Jun 16.

Abstract

Rheumatoid arthritis (RA) fibroblast-like synoviocytes (RA-FLS) play a crucial role in the pathogenesis of RA. RA-FLS display passive pro-inflammatory responses and self-directed aggressive responses, such as pro-inflammatory mediator production, reduced apoptosis and formation of a thickened synovial lining. Evidence suggests a role for Janus kinase (JAK)-signal transducer and transcriptional activator (STAT) signaling in the passive response but the aggressive behavior of RA-FLS is poorly understood. The pharmacologic effects of the novel JAK inhibitor, peficitinib, on cytokine-induced intracellular signaling and self-directed aggressive behavior of RA-FLS (e.g., increased expression of apoptosis-resistant genes and sodium nitroprusside-induced apoptosis) were investigated and compared with approved JAK inhibitors. RA-FLS assembly to form a lining-like structure and pro-inflammatory mediator production was investigated in three-dimensional (3D)-micromass culture. Peficitinib inhibited STAT3 phosphorylation in RA-FLS following induction by interferon (IFN)-α2b, IFN-γ, interleukin (IL)-6, oncostatin M, and leukemia inhibitory factor in a concentration-related manner, and was comparable to approved JAK inhibitors, tofacitinib and baricitinib. Peficitinib and tofacitinib suppressed autocrine phosphorylation of STAT3 and expression of apoptosis-resistant genes, and promoted cell death. In 3D-micromass culture, peficitinib reduced multi-layered RA-FLS cells to a thin monolayer, an effect less pronounced with tofacitinib. Both compounds attenuated production of vascular endothelial growth factor-A, matrix metalloproteinases, IL-6 and tumor necrosis factor superfamily-11. This study confirmed the pathogenic role of uncontrolled JAK-STAT signaling in the aggressive and passive responses of RA-FLS that are critical for RA progression. The novel JAK inhibitor peficitinib suppressed the pro-inflammatory behavior of RA-FLS, accelerated cell death and abrogated thickening of the synovium.

Keywords: Fibroblast-like synoviocytes; Janus kinase; Peficitinib; Rheumatoid arthritis; Signal transducer and activator of transcription.

MeSH terms

  • Adamantane / analogs & derivatives*
  • Adamantane / pharmacology
  • Apoptosis / drug effects
  • Arthritis, Rheumatoid / metabolism*
  • Azetidines / pharmacology
  • Cells, Cultured
  • Cytokines / metabolism
  • Humans
  • Janus Kinase Inhibitors / pharmacology*
  • Janus Kinases / antagonists & inhibitors
  • Janus Kinases / metabolism*
  • Niacinamide / analogs & derivatives*
  • Niacinamide / pharmacology
  • Phosphorylation / drug effects
  • Piperidines / pharmacology
  • Purines / pharmacology
  • Pyrazoles / pharmacology
  • Pyrimidines / pharmacology
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / drug effects
  • Sulfonamides / pharmacology
  • Synoviocytes / drug effects
  • Synoviocytes / metabolism*

Substances

  • Azetidines
  • Cytokines
  • Janus Kinase Inhibitors
  • Piperidines
  • Purines
  • Pyrazoles
  • Pyrimidines
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Sulfonamides
  • Niacinamide
  • tofacitinib
  • Janus Kinases
  • peficitinib
  • baricitinib
  • Adamantane