Role of capsaicin-sensitive nerves and tachykinins in mast cell tryptase-induced inflammation of murine knees

Inflamm Res. 2016 Sep;65(9):725-36. doi: 10.1007/s00011-016-0954-x. Epub 2016 Jun 1.

Abstract

Objective, design: Mast cell tryptase (MCT) is elevated in arthritic joints, but its direct effects are not known. Here, we investigated MCT-evoked acute inflammatory and nociceptive mechanisms with behavioural, in vivo imaging and immunological techniques.

Material and subjects: Neurogenic inflammation involving capsaicin-sensitive afferents, transient receptor potential vanilloid 1 receptor (TRPV1), substance P (SP), neurokinin A (NKA) and their NK1 tachykinin receptor were studied using gene-deleted mice compared to C57Bl/6 wildtypes (n = 5-8/group).

Treatment: MCT was administered intraarticularly or topically (20 μl, 12 μg/ml). Capsaicin-sensitive afferents were defunctionalized with the TRPV1 agonist resiniferatoxin (RTX; 30-70-100 μg/kg s.c. pretreatment).

Methods: Knee diameter was measured with a caliper, synovial perfusion with laser Doppler imaging, mechanonociception with aesthesiometry and weight distribution with incapacitance tester over 6 h. Cytokines and neuropeptides were determined with immunoassays.

Results: MCT induced synovial vasodilatation, oedema, impaired weight distribution and mechanical hyperalgesia, but cytokine or neuropeptide levels were not altered at the 6-h timepoint. Hyperaemia was reduced in RTX-treated and TRPV1-deleted animals, and oedema was absent in NK1-deficient mice. Hyperalgesia was decreased in SP/NKA- and NK1-deficient mice, weight bearing impairment in RTX-pretreated, TRPV1- and NK1-deficient animals.

Conclusions: MCT evokes synovial hyperaemia, oedema, hyperalgesia and spontaneous pain. Capsaicin-sensitive afferents and TRPV1 receptors are essential for vasodilatation, while tachykinins mediate oedema and pain.

Keywords: Arthritis; Capsaicin-sensitive sensory nerves; Inflammation; Oedema; Pain; Synovial microcirculation.

MeSH terms

  • Animals
  • Arthritis / chemically induced*
  • Arthritis / metabolism
  • Calcitonin Gene-Related Peptide / metabolism
  • Capsaicin
  • Cytokines / metabolism
  • Edema / chemically induced*
  • Edema / metabolism
  • Edema / pathology
  • Hyperalgesia / chemically induced*
  • Hyperalgesia / metabolism
  • Hyperalgesia / pathology
  • Knee Joint / metabolism
  • Knee Joint / pathology
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurogenic Inflammation / chemically induced*
  • Neurogenic Inflammation / metabolism
  • Neurogenic Inflammation / pathology
  • Pain / chemically induced*
  • Pain / metabolism
  • Pain / pathology
  • Protein Precursors / genetics
  • Receptor, PAR-2 / metabolism
  • Receptors, Neurokinin-1 / genetics
  • Substance P / metabolism
  • TRPV Cation Channels / genetics
  • Tachykinins / genetics
  • Touch
  • Tryptases*

Substances

  • Cytokines
  • Protein Precursors
  • Receptor, PAR-2
  • Receptors, Neurokinin-1
  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • Tachykinins
  • preprotachykinin
  • Substance P
  • Tryptases
  • Calcitonin Gene-Related Peptide
  • Capsaicin