A new copper ionophore DPMQ protects cells against ultraviolet B irradiation by inhibiting the TRPV1 channel

J Cell Physiol. 2018 Dec;233(12):9594-9610. doi: 10.1002/jcp.26861. Epub 2018 Jun 26.

Abstract

Copper is more likely than iron to generate reactive oxygen species (ROS) in a redox reaction due to its higher electrochemical reactivity. This study examined the effect of a newly synthesized Cu2+ binding compound, (E)-2-(4-(dimethylamino)phenylimino)methyl)quinolin-8-ol (DPMQ), on ultraviolet B (UVB) irradiation-induced cytotoxicity in human dermal fibroblasts. DPMQ induced Cu2+ influx as effectively as disulfiram, a Cu2+ ionophore anticancer drug. However, disulfiram induced ROS generation, mitochondrial dysfunction, and apoptosis in fibroblasts in a Cu2+ -dependent manner, whereas DPMQ was not only nontoxic, but protected cells against UVB irradiation-induced apoptosis in a Cu2+ -independent manner. UVB irradiation induced a Ca2+ -dependent increase in ROS generation, a decrease in Nrf2 levels, and activation of the mitochondrial apoptotic pathway, and these effects were prevented by DPMQ, which also increased Nrf2 nuclear translocation in a Cu2+ -independent manner. UVB irradiation activated 12-lipoxygenase and 12-hydroxyeicosatetraenoic acid (12-HETE), a product of 12-lipoxygenase, activated the TRPV1 channel. DMPQ did not act as a Ca2+ chelator, but inhibited the cytosolic Ca2+ increase induced by 12-HETE or capsaicin, but not that induced by bradykinin or ATP. Blockade of Ca2+ influx by pharmacological inhibition or silencing of the TRPV1 channel or chelation of cytosolic Ca2+ inhibited the UVB irradiation-induced Nrf2 reduction, ROS generation, mitochondrial dysfunction, and apoptosis. Taken together, our results suggest that Ca2+ influx via the TRPV1 channel is responsible for UVB irradiation-induced cytotoxicity and that DPMQ protects cells against UVB irradiation by inhibiting the TRPV1 channel and stabilizing Nrf2, and could thus be a potentially useful compound for the treatment of free radical-induced diseases.

Keywords: Nrf2; TRPV1 channel; cytosolic calcium concentration; reactive oxygen species; ultraviolet B irradiation..

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylcysteine / pharmacology
  • Apoptosis / drug effects
  • Apoptosis / radiation effects
  • Arachidonate 12-Lipoxygenase / metabolism
  • Caspase 3 / metabolism
  • Cell Proliferation / drug effects
  • Cell Proliferation / radiation effects
  • Copper / pharmacology*
  • Cytoprotection* / drug effects
  • Cytoprotection* / radiation effects
  • Dermis / cytology
  • Disulfiram / pharmacology
  • Enzyme Activation / drug effects
  • Enzyme Activation / radiation effects
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibroblasts / radiation effects
  • Gene Silencing / drug effects
  • Gene Silencing / radiation effects
  • Humans
  • Ion Channel Gating / drug effects
  • Ion Channel Gating / radiation effects
  • Ionophores / pharmacology*
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitochondria / radiation effects
  • NF-E2-Related Factor 2 / metabolism
  • Protective Agents / pharmacology
  • Quinolines / pharmacology*
  • Reactive Oxygen Species / metabolism
  • TRPV Cation Channels / metabolism*
  • Ultraviolet Rays*

Substances

  • Ionophores
  • NF-E2-Related Factor 2
  • NFE2L2 protein, human
  • Protective Agents
  • Quinolines
  • Reactive Oxygen Species
  • TRPV Cation Channels
  • TRPV1 protein, human
  • Copper
  • Arachidonate 12-Lipoxygenase
  • Caspase 3
  • Disulfiram
  • Acetylcysteine