Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury

J Neurochem. 2006 May;97(3):772-83. doi: 10.1111/j.1471-4159.2006.03746.x. Epub 2006 Mar 8.

Abstract

Peripheral nerve injury can induce spinal microglial/astrocyte activation. Substances released by activated glial cells excite spinal nociceptive neurons. Pharmacological disruption of glial activation or antagonism of substances released by activated glia prevent or reverse pain hypersensitivity. It is not known, however, what causes spinal cord glia to shift from a resting to an activated state. In an attempt to understand the potential role of monocyte chemoattractant protein-1 (MCP-1) in triggering spinal glial activation and its contribution to the development of neuropathic pain, we investigated the effect of peripheral nerve injury on MCP-1 expression in dorsal root ganglia (DRG) and the spinal cord, and established its temporal relationship with activation of spinal microglia and astrocytes. We observed that MCP-1 was induced by chronic constriction of the sciatic nerve in DRG sensory neurons, spinal cord motor neurons and in the superficial dorsal horn, ipsilateral to the injury. Neuronal MCP-1 induction was followed by surrounding microglial activation. After peaking at day 7 after injury, MCP-1 levels began to decline rapidly and had returned to baseline by day 150. In contrast, microglial activation peaked by day 14 and declined afterwards to reach a lower, yet significantly raised level beyond day 22 and remained increased until the end of the test period. Astrocyte activation became detectable later, progressed more slowly and also remained increased until the end of the test period, in parallel with a decreased nociceptive threshold. Our results suggest that neuronal MCP-1 may serve as a trigger for spinal microglial activation, which participates in the initiation of neuropathic pain. Delayed, sustained astrocyte activation may participate with microglia in the persistent phase of pain hypersensitivity.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 3 / genetics
  • Activating Transcription Factor 3 / metabolism
  • Animals
  • CD11b Antigen / metabolism
  • Calcitonin Gene-Related Peptide / metabolism
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism*
  • Disease Models, Animal
  • Functional Laterality
  • Ganglia, Spinal / metabolism
  • Ganglia, Spinal / pathology*
  • Glial Fibrillary Acidic Protein / metabolism
  • Immunohistochemistry / methods
  • In Situ Hybridization / methods
  • Male
  • Neuroglia / physiology*
  • Pain Measurement / methods
  • Pain Threshold / physiology
  • Peripheral Nervous System Diseases / metabolism*
  • Peripheral Nervous System Diseases / pathology*
  • Peripheral Nervous System Diseases / physiopathology
  • Phosphopyruvate Hydratase / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Time Factors

Substances

  • Activating Transcription Factor 3
  • Atf3 protein, rat
  • CD11b Antigen
  • Ccl2 protein, rat
  • Chemokine CCL2
  • Glial Fibrillary Acidic Protein
  • Phosphopyruvate Hydratase
  • Calcitonin Gene-Related Peptide