Activation of spinal Extacellular Signal-Regulated Kinases and c-jun N-terminal kinase signaling pathways contributes to morphine-induced acute and chronic hyperalgesia in mice

J Cell Biochem. 2019 Sep;120(9):15045-15056. doi: 10.1002/jcb.28766. Epub 2019 Apr 23.

Abstract

Background: This study investigated the activation of mitogen-activated protein kinases in the spinal dorsal horn to explore the mechanisms underlying morphine-induced acute and chronic hyperalgesia in mice.

Methods: Male adult mice were given a single subcutaneous injection (SC) of morphine (1 μg/kg) or twice-daily administration of morphine (10 mg/kg/day) for 8 days. Thermal hyperalgesia and mechanical allodynia were assessed using the radiant heat and von Frey filament test. Levels of phospho (p)-extracellular signal-regulated kinases (p-ERK), p-c-Jun N-terminal kinase (p-JNK), p-p38, p-PKCγ, N-methyl-d-aspartate receptor (NMDAr), and c-Fos protein in the spinal dorsal horn were examined by Western blot assays.

Results: A single ultra-low dose or repeated administration of morphine induced hyperalgesia in mice and caused a significant increase in the levels of p-ERK and p-JNK, but not p-p38, in the spinal dorsal horn. The level of c-Fos protein was significantly elevated following administration of morphine. The protein levels of p-PKCγ and NMDAr subunits (NR2B and NR2A) were also altered. Pretreatment with the NMDAr antagonist MK-801 or the protein kinase C (PKC) inhibitor calphostin C (CC) suppressed the morphine-induced increase in p-ERK, p-JNK, and c-Fos. Administration of MK-801 and CC also relieved morphine-induced hyperalgesia.

Conclusion: These findings suggest that activation of the spinal ERK and JNK signaling pathways contribute to morphine-induced acute and chronic hyperalgesia in mice.

Keywords: acute hyperalgesia; c-Jun N-terminal kinase; chronic hyperalgesia; extracellular signal-regulated kinases; morphine.

MeSH terms

  • Analgesics, Opioid / pharmacology*
  • Animals
  • Enzyme Activation
  • Extracellular Signal-Regulated MAP Kinases / metabolism*
  • Hyperalgesia / chemically induced*
  • JNK Mitogen-Activated Protein Kinases / metabolism*
  • MAP Kinase Signaling System / physiology
  • Male
  • Mice
  • Morphine / pharmacology*
  • Protein Kinase C / metabolism
  • Proto-Oncogene Proteins c-fos / metabolism
  • Receptors, N-Methyl-D-Aspartate / agonists
  • Spinal Cord Dorsal Horn / metabolism*
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Analgesics, Opioid
  • Proto-Oncogene Proteins c-fos
  • Receptors, N-Methyl-D-Aspartate
  • Morphine
  • Protein Kinase C
  • Extracellular Signal-Regulated MAP Kinases
  • JNK Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases