Interleukin-17 sensitizes joint nociceptors to mechanical stimuli and contributes to arthritic pain through neuronal interleukin-17 receptors in rodents

Arthritis Rheum. 2012 Dec;64(12):4125-34. doi: 10.1002/art.37695.

Abstract

Objective: Interleukin-17 (IL-17) is considered a proinflammatory cytokine, but whether neuronal IL-17 receptors contribute to the generation of arthritic pain is unknown. This study was undertaken to explore whether IL-17A acts on neurons, whether it sensitizes joint nociceptors, and whether neutralization of IL-17 is antinociceptive.

Methods: We recorded action potentials from rat joint nociceptors after intraarticular injection of IL-17A. We studied the expression of the IL-17A receptor in the rat dorsal root ganglia (DRG), explored the effect of IL-17A on signaling pathways in cultured rat DRG neurons, and using patch clamp recordings, monitored changes of excitability by IL-17A. We tested whether an antibody to IL-17 influences pain behaviors in mice with antigen-induced arthritis (AIA).

Results: A single injection of IL-17A into the rat knee joint elicited a slowly developing and long-lasting sensitization of nociceptive C fibers of the joint to mechanical stimuli, which was not attenuated by neutralizing tumor necrosis factor α or IL-6. The IL-17A receptor was visualized in most rat DRG neurons, the cell bodies of primary sensory neurons. In isolated and cultured rat DRG neurons, IL-17A caused rapid phosphorylation of protein kinase B and ERK, and it rapidly enhanced excitability. In mice with unilateral AIA in the knee, an antibody against IL-17 improved the guarding score and reduced secondary mechanical hyperalgesia at the ipsilateral paw.

Conclusion: Our findings indicate that IL-17A has the potential to act as a pain mediator by targeting IL-17 receptors in nociceptive neurons, and these receptors are particularly involved in inflammation-evoked mechanical hyperalgesia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / immunology
  • Antibodies, Monoclonal / therapeutic use
  • Antigens / adverse effects
  • Arthritis, Experimental / chemically induced
  • Arthritis, Experimental / complications
  • Arthritis, Experimental / physiopathology*
  • Cells, Cultured
  • Disease Models, Animal
  • Extracellular Signal-Regulated MAP Kinases
  • Ganglia, Spinal / metabolism
  • Ganglia, Spinal / pathology
  • Ganglia, Spinal / physiopathology
  • Hyperalgesia / physiopathology*
  • Injections, Intra-Articular
  • Interleukin-17 / administration & dosage
  • Interleukin-17 / immunology
  • Interleukin-17 / pharmacology*
  • Knee Joint / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons / physiology*
  • Nociceptors / drug effects*
  • Nociceptors / physiology
  • Pain / drug therapy
  • Pain / etiology
  • Pain / physiopathology*
  • Patch-Clamp Techniques
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Rats, Wistar
  • Receptors, Interleukin-17 / physiology*

Substances

  • Antibodies, Monoclonal
  • Antigens
  • Interleukin-17
  • Receptors, Interleukin-17
  • Proto-Oncogene Proteins c-akt
  • Extracellular Signal-Regulated MAP Kinases