Role of extracellular signal-regulated kinase in the ventral tegmental area in the suppression of the morphine-induced rewarding effect in mice with sciatic nerve ligation

J Neurochem. 2004 Mar;88(6):1389-97. doi: 10.1046/j.1471-4159.2003.02272.x.

Abstract

We recently reported that micro-opioid receptor agonist morphine failed to induce its rewarding effects in rodents with sciatic nerve injury. In the present study, we investigated whether a state of neuropathic pain induced by sciatic nerve ligation could change the activities of the extracellular signal-regulated kinase (ERK) and p38 in the mouse lower midbrain area including the ventral tegmental area (VTA), and these changes could directly affect the development of the morphine-induced rewarding effect in mice. The sciatic nerve ligation caused a long-lasting and profound thermal hyperalgesia. A dose-dependent place preference induced by s.c. administration of morphine was observed in sham-operated mice, but not in sciatic nerve-ligated mice. We found here for the first time that nerve injury produces a sustained and significant reduction in protein levels of phosphorylated-ERK and -p38 in cytosolic preparations of the mouse lower midbrain. The inhibition of ERK activity by i.c.v. pre-treatment with either PD98059 or U0126 impaired the morphine-induced place preference. In contrast, i.c.v. treatment with a specific inhibitor of p38, SB203580, did not interfere with the morphine-induced rewarding effect. Immunohistochemical study showed a drastic reduction in phosphorylated-ERK immunoreactivity within tyrosine hydroxylase-positive cells of the VTA. These results suggest that a sustained reduction in the ERK-dependent signalling pathway in dopamine cells of the VTA may be implicated in the suppression of the morphine-induced rewarding effect under neuropathic pain.

MeSH terms

  • Analgesics, Opioid / pharmacology
  • Animals
  • Cytosol / enzymology
  • Disease Models, Animal
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Hyperalgesia / drug therapy
  • Hyperalgesia / enzymology
  • Hyperalgesia / etiology
  • Ligation
  • Male
  • Mesencephalon / chemistry
  • Mesencephalon / drug effects
  • Mesencephalon / enzymology
  • Mice
  • Mice, Inbred ICR
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / metabolism*
  • Morphine / pharmacology*
  • Neurons / drug effects
  • Neurons / enzymology
  • Phosphorylation
  • Receptors, Opioid, mu / agonists
  • Reward*
  • Sciatic Neuropathy / complications
  • Sciatic Neuropathy / drug therapy
  • Sciatic Neuropathy / physiopathology*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Spatial Behavior / drug effects
  • Tyrosine 3-Monooxygenase / biosynthesis
  • Ventral Tegmental Area / cytology
  • Ventral Tegmental Area / drug effects
  • Ventral Tegmental Area / enzymology*
  • p38 Mitogen-Activated Protein Kinases

Substances

  • Analgesics, Opioid
  • Enzyme Inhibitors
  • Receptors, Opioid, mu
  • Morphine
  • Tyrosine 3-Monooxygenase
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases