IL-33/ST2 induces neutrophil-dependent reactive oxygen species production and mediates gout pain

Theranostics. 2020 Oct 27;10(26):12189-12203. doi: 10.7150/thno.48028. eCollection 2020.

Abstract

Objective: Gout, induced by monosodium urate (MSU) crystal deposition in joint tissues, provokes severe pain and impacts life quality of patients. However, the mechanisms underlying gout pain are still incompletely understood. Methods: We established a mouse gout model by intra-articularly injection of MSU crystals into the ankle joint of wild type and genetic knockout mice. RNA-Sequencing, in vivo molecular imaging, Ca2+ imaging, reactive oxygen species (ROS) generation, neutrophil influx and nocifensive behavioral assays, etc. were used. Results: We found interleukin-33 (IL-33) was among the top up-regulated cytokines in the inflamed ankle. Neutralizing or genetic deletion of IL-33 or its receptor ST2 (suppression of tumorigenicity) significantly ameliorated pain hypersensitivities and inflammation. Mechanistically, IL-33 was largely released from infiltrated macrophages in inflamed ankle upon MSU stimulation. IL-33 promoted neutrophil influx and triggered neutrophil-dependent ROS production via ST2 during gout, which in turn, activated transient receptor potential ankyrin 1 (TRPA1) channel in dorsal root ganglion (DRG) neurons and produced nociception. Further, TRPA1 channel activity was significantly enhanced in DRG neurons that innervate the inflamed ankle via ST2 dependent mechanism, which results in exaggerated nociceptive response to endogenous ROS products during gout. Conclusions: We demonstrated a previous unidentified role of IL-33/ST2 in mediating pain hypersensitivity and inflammation in a mouse gout model through promoting neutrophil-dependent ROS production and TRPA1 channel activation. Targeting IL-33/ST2 may represent a novel therapeutic approach to ameliorate gout pain and inflammation.

Keywords: Gout; TRPA1; arthritis; cytokine; neutrophil; reactive oxygen species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Disease Models, Animal
  • Gout / chemically induced
  • Gout / complications*
  • Gout / immunology
  • Gout / pathology
  • Humans
  • Injections, Intra-Articular
  • Interleukin-1 Receptor-Like 1 Protein / genetics
  • Interleukin-1 Receptor-Like 1 Protein / metabolism*
  • Interleukin-33 / genetics
  • Interleukin-33 / metabolism*
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Knockout
  • Neutrophils / immunology*
  • Neutrophils / metabolism
  • Pain / immunology*
  • Pain / pathology
  • RAW 264.7 Cells
  • RNA-Seq
  • Reactive Oxygen Species
  • TRPA1 Cation Channel / metabolism
  • Tarsal Joints / immunology
  • Tarsal Joints / pathology
  • Uric Acid / administration & dosage

Substances

  • Il1rl1 protein, mouse
  • Il33 protein, mouse
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • Reactive Oxygen Species
  • TRPA1 Cation Channel
  • Trpa1 protein, mouse
  • Uric Acid