Activation of PKCε-ALDH2 Axis Prevents 4-HNE-Induced Pain in Mice

Biomolecules. 2021 Nov 30;11(12):1798. doi: 10.3390/biom11121798.

Abstract

Protein kinase Cε (PKCε) is highly expressed in nociceptor neurons and its activation has been reported as pro-nociceptive. Intriguingly, we previously demonstrated that activation of the mitochondrial PKCε substrate aldehyde dehydrogenase-2 (ALDH2) results in anti-nociceptive effects. ALDH2 is a major enzyme responsible for the clearance of 4-hydroxy-2-nonenal (4-HNE), an oxidative stress byproduct accumulated in inflammatory conditions and sufficient to induce pain hypersensitivity in rodents. Here we determined the contribution of the PKCε-ALDH2 axis during 4-HNE-induced mechanical hypersensitivity. Using knockout mice, we demonstrated that PKCε is essential for the nociception recovery during 4-HNE-induced hypersensitivity. We also found that ALDH2 deficient knockin mice display increased 4-HNE-induced nociceptive behavior. As proof of concept, the use of a selective peptide activator of PKCε (ΨεHSP90), which favors PKCε translocation to mitochondria and activation of PKCε-ALDH2 axis, was sufficient to block 4-HNE-induced hypersensitivity in WT, but not in ALDH2-deficient mice. Similarly, ΨεHSP90 administration prevented mechanical hypersensitivity induced by endogenous production of 4-HNE after carrageenan injection. These findings provide evidence that selective activation of mitochondrial PKCε-ALDH2 axis is important to mitigate aldehyde-mediated pain in rodents, suggesting that ΨεHSP90 and small molecules that mimic it may be a potential treatment for patients with pain.

Keywords: hyperalgesia; neurodegeneration; neuroprotection; oxidative stress; protein kinase.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldehyde Dehydrogenase, Mitochondrial / genetics*
  • Aldehyde Dehydrogenase, Mitochondrial / metabolism
  • Aldehydes / adverse effects*
  • Animals
  • Carrageenan / adverse effects
  • Disease Models, Animal
  • Gene Knock-In Techniques
  • Gene Knockout Techniques
  • Male
  • Mice
  • Mitochondria / metabolism
  • Pain / chemically induced
  • Pain / metabolism*
  • Protein Kinase C-epsilon / metabolism*
  • Protein Transport

Substances

  • Aldehydes
  • Carrageenan
  • ALDH2 protein, mouse
  • Aldehyde Dehydrogenase, Mitochondrial
  • Prkce protein, mouse
  • Protein Kinase C-epsilon
  • 4-hydroxy-2-nonenal