Dynamic regulation of spinal pro-inflammatory cytokine release in the rat in vivo following peripheral nerve injury

Brain Behav Immun. 2010 May;24(4):569-76. doi: 10.1016/j.bbi.2009.12.007. Epub 2009 Dec 24.

Abstract

Spinal release of cytokines may play a critical role in the maladapted nociceptive signaling underlying chronic pain states. In order to investigate this biology, we have developed a novel 'high flux' intrathecal microdialysis approach in combination with multiplex bead-based immunoassay technology to concurrently monitor the spinal release of interleukin (IL)-1beta, IL-6 and tumour necrosis factor (TNF)alpha in rats with unilateral sciatic nerve chronic constriction injury (CCI). Intrathecal microdialysis was performed under isoflurane/N(2)O anaesthesia in rats with confirmed mechanical hypersensitivity. In a first study, C-fiber strength electrical stimulation of the operated nerve in neuropathic rats was found to evoke a dramatic increase in IL-1beta efflux ( approximately 15-fold) that was significantly greater than that observed in the sham-operated group. Spinal IL-6 efflux was also responsive to primary afferent stimulation, whereas TNFalpha was not. In a second study, treatment with the glial inhibitor propentofylline for 7days normalized CCI-induced mechanical hypersensitivity. In the same animals, this treatment also significantly reduced intrathecal IL-1beta, IL-6 and TNFalpha and prevented afferent stimulation-evoked cytokine release of both IL-1beta and IL-6. These results provide support for glia as the source of the majority of intrathecal IL-1beta, IL-6 and TNFalpha that accompanies mechanical hypersensitivity in the CCI rat. Moreover, our studies demonstrate the ability of a neurone-glia signaling mechanism to dynamically modulate this release and support a role of spinal IL-1beta in the phasic transmission of abnormal pain signals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afferent Pathways
  • Animals
  • Cytokines / metabolism*
  • Disease Models, Animal
  • Electric Stimulation / methods
  • Interleukin-1beta / metabolism*
  • Interleukin-6 / metabolism*
  • Male
  • Microdialysis / methods
  • Neuroglia / drug effects
  • Neuroglia / immunology
  • Neuroprotective Agents / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Sciatic Nerve / injuries
  • Spinal Cord / drug effects
  • Spinal Cord / immunology*
  • Trauma, Nervous System / immunology*
  • Tumor Necrosis Factor-alpha / metabolism*
  • Xanthines / pharmacology

Substances

  • Cytokines
  • Interleukin-1beta
  • Interleukin-6
  • Neuroprotective Agents
  • Tumor Necrosis Factor-alpha
  • Xanthines
  • propentofylline