Spinal TLR4 mediates the transition to a persistent mechanical hypersensitivity after the resolution of inflammation in serum-transferred arthritis

Pain. 2011 Dec;152(12):2881-2891. doi: 10.1016/j.pain.2011.09.020. Epub 2011 Oct 21.

Abstract

Persistent pain after resolution of clinically appreciable signs of arthritis poses a therapeutic challenge, and immunosuppressive therapies do not meet this medical need. To investigate this conversion to persistent pain, we utilized the K/BxN serum transfer arthritis model, which has persistent mechanical hypersensitivity despite the resolution of visible inflammation. Toll-like receptor (TLR) 4 has been implicated as a potential therapeutic target in neuropathic and other pain models. We compared the relative courses of serum transfer arthritis and mechanical hypersensitivity in wild type (WT) and Tlr4(-/-) mice. K/BxN serum transfer induced similar joint swelling and inflammation from days 4-22 in WT and Tlr4(-/-) mice. Unlike WT mice, Tlr4(-/-) mice displayed a significant reversal in mechanical hypersensitivity and diminished appearance of glial activation markers after resolution of peripheral inflammation. Intrathecal (IT) delivery of a TLR4 antagonist, lipopolysaccharide Rhodobacter sphaeroides (LPS-RS; 10 μg), on days 6, 9, and 12 abrogated the transition to persistent mechanical hypersensitivity in WT arthritic mice, while later administration had no impact. We utilized a lipidomics liquid chromatography tandem mass spectrometry methodology to determine spinal cord profiles of bioactive lipid species after early LPS-RS treatment compared to vehicle-treated control animals. WT arthritic mice had reduced spinal levels of the anti-inflammatory prostaglandin 15-deoxy-Δ(12,14)-PGJ(2) (15d-PGJ(2)) on day 6, compared to IT LPS-RS-treated mice. Direct IT application of 15d-PGJ(2) (0.5 μg) on day 6 improved mechanical hypersensitivity in arthritic mice within 15 min. Hence, TLR4 signaling altered spinal bioactive lipid profiles in the serum transfer model and played a critical role in the transition from acute to chronic postinflammatory mechanical hypersensitivity.

Publication types

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

MeSH terms

  • Animals
  • Arthritis, Experimental / blood
  • Arthritis, Experimental / immunology
  • Arthritis, Experimental / pathology*
  • Chronic Pain / blood
  • Chronic Pain / immunology
  • Chronic Pain / pathology*
  • Disease Models, Animal
  • Hyperalgesia / blood
  • Hyperalgesia / immunology
  • Hyperalgesia / pathology*
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / blood
  • Inflammation Mediators / physiology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Signal Transduction / immunology
  • Spinal Cord / immunology*
  • Spinal Cord / metabolism
  • Spinal Cord / pathology
  • Toll-Like Receptor 4 / antagonists & inhibitors
  • Toll-Like Receptor 4 / deficiency
  • Toll-Like Receptor 4 / physiology*

Substances

  • Inflammation Mediators
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4