In vivo recruitment by painful stimuli of AMPA receptor subunits to the plasma membrane of spinal cord neurons

Pain. 2004 Dec;112(3):315-323. doi: 10.1016/j.pain.2004.09.011.

Abstract

The persistent increase in pain sensitivity observed after injury, known as hyperalgesia, depends on synaptic plasticity in the pain pathway, particularly in the spinal cord. Several potential mechanisms have been proposed, including post-synaptic exocytosis of the AMPA subclass of glutamate receptors (AMPA-R), which is known to play a critical role in synaptic plasticity in the hippocampus. AMPA-R trafficking has been described in spinal neurons in culture but it is unknown if it can also occur in spinal neurons in vivo, or if it can be induced by natural painful stimulation. Here we have induced referred mechanical hyperalgesia in vivo by intracolonic instillation of capsaicin in mice and have observed a recruitment of GluR1 AMPA-R subunits to neuronal plasma membranes in the lumbar spinal cord. Intracolonic capsaicin induced a rapid (10 min) increase in GluR1, but not GluR2/3 in the synaptosomal membrane fraction which lasted at least 3 h and a decrease in GluR1 subunit in the cytosolic fraction. Capsaicin treatment also provoked CaMKII activation and pre-treatment with a specific CaMKII inhibitor prevented the GluR1 trafficking. Brefeldin-A, an antibiotic that inhibits exocytosis of proteins, not only prevented GluR1 trafficking to the membrane but also inhibited referred hyperalgesia in capsaicin-treated mice. Our results show that delivery of GluR1 AMPA receptor subunits to the cell membrane through a CaMKII activity-dependent exocytotic regulated pathway contributes to the development of hyperalgesia after a painful stimulus. We conclude that AMPA-R trafficking contributes to the synaptic strengthening induced in the pain pathway by natural stimulation.

Publication types

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

MeSH terms

  • Animals
  • Behavior, Animal
  • Benzylamines / pharmacology
  • Blotting, Western / methods
  • Brefeldin A / pharmacology
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism
  • Capsaicin / pharmacology
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism*
  • Cytosol / drug effects
  • Cytosol / metabolism
  • Drug Interactions
  • Hyperalgesia / metabolism*
  • Hyperalgesia / physiopathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neurons / cytology*
  • Neurons / drug effects
  • Physical Stimulation / methods
  • Protein Kinase Inhibitors / pharmacology
  • Protein Synthesis Inhibitors / pharmacology
  • Receptors, AMPA / metabolism*
  • Spinal Cord / cytology*
  • Sulfonamides / pharmacology
  • Time Factors

Substances

  • Benzylamines
  • Protein Kinase Inhibitors
  • Protein Synthesis Inhibitors
  • Receptors, AMPA
  • Sulfonamides
  • KN 93
  • Brefeldin A
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Capsaicin
  • glutamate receptor ionotropic, AMPA 1