Gabapentin Effects on PKC-ERK1/2 Signaling in the Spinal Cord of Rats with Formalin-Induced Visceral Inflammatory Pain

PLoS One. 2015 Oct 29;10(10):e0141142. doi: 10.1371/journal.pone.0141142. eCollection 2015.

Abstract

Currently, the clinical management of visceral pain remains unsatisfactory for many patients suffering from this disease. While preliminary animal studies have suggested the effectiveness of gabapentin in successfully treating visceral pain, the mechanism underlying its analgesic effect remains unclear. Evidence from other studies has demonstrated the involvement of protein kinase C (PKC) and extracellular signal-regulated kinase1/2 (ERK1/2) in the pathogenesis of visceral inflammatory pain. In this study, we tested the hypothesis that gabapentin produces analgesia for visceral inflammatory pain through its inhibitory effect on the PKC-ERK1/2 signaling pathway. Intracolonic injections of formalin were performed in rats to produce colitis pain. Our results showed that visceral pain behaviors in these rats decreased after intraperitoneal injection of gabapentin. These behaviors were also reduced by intrathecal injections of the PKC inhibitor, H-7, and the ERK1/2 inhibitor, PD98059. Neuronal firing of wide dynamic range neurons in L6-S1 of the rat spinal cord dorsal horn were significantly increased after intracolonic injection of formalin. This increased firing rate was inhibited by intraperitoneal injection of gabapentin and both the individual and combined intrathecal application of H-7 and PD98059. Western blot analysis also revealed that PKC membrane translocation and ERK1/2 phosphorylation increased significantly following formalin injection, confirming the recruitment of PKC and ERK1/2 during visceral inflammatory pain. These effects were also significantly reduced by intraperitoneal injection of gabapentin. Therefore, we concluded that the analgesic effect of gabapentin on visceral inflammatory pain is mediated through suppression of PKC and ERK1/2 signaling pathways. Furthermore, we found that the PKC inhibitor, H-7, significantly diminished ERK1/2 phosphorylation levels, implicating the involvement of PKC and ERK1/2 in the same signaling pathway. Thus, our results suggest a novel mechanism of gabapentin-mediated analgesia for visceral inflammatory pain through a PKC-ERK1/2 signaling pathway that may be a future therapeutic target for the treatment of visceral inflammatory pain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine / pharmacology
  • Amines / pharmacology*
  • Animals
  • Behavior, Animal
  • Cell Membrane / metabolism
  • Cyclohexanecarboxylic Acids / pharmacology*
  • Disease Models, Animal
  • Electrophysiological Phenomena
  • Flavonoids / pharmacology
  • Formaldehyde / adverse effects
  • Gabapentin
  • MAP Kinase Signaling System / drug effects*
  • Male
  • Neurons / drug effects
  • Neurons / physiology
  • Pain Management
  • Phosphorylation
  • Protein Kinase C / metabolism*
  • Protein Transport
  • Rats
  • Spinal Cord / drug effects*
  • Spinal Cord / metabolism*
  • Visceral Pain / drug therapy
  • Visceral Pain / etiology*
  • Visceral Pain / metabolism*
  • gamma-Aminobutyric Acid / pharmacology*

Substances

  • Amines
  • Cyclohexanecarboxylic Acids
  • Flavonoids
  • Formaldehyde
  • gamma-Aminobutyric Acid
  • Gabapentin
  • 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine
  • Protein Kinase C
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one

Grants and funding

This study was supported by the National Science and Technology Support Program in China (2013BAI07B01), the Natural Science Foundation of Shandong Province in China (ZR2012HQ014, ZR2011HM044), and Shandong Province Medical and Health Plan (2014WSB32015). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.