Inhibitor kappa B kinase beta dependent cytokine upregulation in nociceptive neurons contributes to nociceptive hypersensitivity after sciatic nerve injury

J Pain. 2012 May;13(5):485-97. doi: 10.1016/j.jpain.2012.02.010.

Abstract

Inhibitor kappa B kinase (IKK)-mediated nuclear factor-kappa B (NF-κB) activation is a major pathway for transcriptional control of various pro-inflammatory factors. We here assessed whether activation of this pathway specifically in primary nociceptive neurons of the dorsal root ganglia (DRG) contributes to the development of nociceptive hypersensitivity. Mice carrying a cre-loxP-mediated deletion of inhibitor kappa B kinase beta (IKKβ) in DRG neurons were protected from nerve injury-evoked allodynia and hyperalgesia. This effect was mimicked by systemic treatment with an IKKβ inhibitor but was not observed upon specific inhibition of IKKβ in the spinal cord, suggesting a specific role of IKKβ in the peripheral neurons. The deletion of IKKβ in DRG neurons did not affect constitutive neuronal NF-κB activity, but reduced nerve injury-evoked NF-κB stimulation in the DRG and was associated with reduced upregulation of interleukin-16, monocyte chemoattractant protein-1/chemokine (CC motif) ligand 2 (MCP-1/CCL2), and tumor necrosis factor alpha (TNFα) in the DRG. These cytokines evoked a rapid rise of intracellular calcium in subsets of primary DRG neurons. The results suggest that IKKβ-mediated NF-κB stimulation in injured primary sensory neurons promotes cytokine and chemokine production and contributes thereby to the development of chronic pain.

Perspective: Inhibitors of IKK that do not pass the blood-brain barrier and act only in the periphery might be useful for reduction of the pro-inflammatory response in peripheral DRG neurons and reduce thereby nerve injury-evoked pain without affecting neuroprotective effects of NF-κB in the central nervous system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Calcium / metabolism
  • Cells, Cultured
  • Cytokines / genetics
  • Cytokines / metabolism*
  • Cytokines / pharmacology
  • Disease Models, Animal
  • Drug Delivery Systems
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use
  • Ganglia, Spinal / pathology*
  • Hyperalgesia / drug therapy
  • Hyperalgesia / etiology*
  • Hyperalgesia / genetics
  • I-kappa B Kinase / deficiency
  • I-kappa B Kinase / metabolism*
  • I-kappa B Kinase / therapeutic use
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nociceptors / drug effects
  • Nociceptors / metabolism*
  • Pain Threshold / drug effects
  • Reaction Time / drug effects
  • Reaction Time / genetics
  • Sciatic Neuropathy / complications
  • Sciatic Neuropathy / drug therapy
  • Sciatic Neuropathy / pathology*
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism
  • Spinal Cord / pathology
  • Time Factors
  • Up-Regulation / drug effects
  • Up-Regulation / genetics
  • Up-Regulation / physiology*

Substances

  • Cytokines
  • Enzyme Inhibitors
  • I-kappa B Kinase
  • Calcium