The Mechanosensitive Ion Channel Piezo Inhibits Axon Regeneration

Neuron. 2019 Apr 17;102(2):373-389.e6. doi: 10.1016/j.neuron.2019.01.050. Epub 2019 Feb 25.

Abstract

Neurons exhibit a limited ability of repair. Given that mechanical forces affect neuronal outgrowth, it is important to investigate whether mechanosensitive ion channels may regulate axon regeneration. Here, we show that DmPiezo, a Ca2+-permeable non-selective cation channel, functions as an intrinsic inhibitor for axon regeneration in Drosophila. DmPiezo activation during axon regeneration induces local Ca2+ transients at the growth cone, leading to activation of nitric oxide synthase and the downstream cGMP kinase Foraging or PKG to restrict axon regrowth. Loss of DmPiezo enhances axon regeneration of sensory neurons in the peripheral and CNS. Conditional knockout of its mammalian homolog Piezo1 in vivo accelerates regeneration, while its pharmacological activation in vitro modestly reduces regeneration, suggesting the role of Piezo in inhibiting regeneration may be evolutionarily conserved. These findings provide a precedent for the involvement of mechanosensitive channels in axon regeneration and add a potential target for modulating nervous system repair.

Keywords: Drosophila; Piezo; axon regeneration; corneal sensory nerve; dendritic arborization neurons; ion channels; mammalian injury model; mechanosensitive; nitric oxide synthase.

Publication types

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

MeSH terms

  • Animals
  • Axons / physiology*
  • Calcium / metabolism
  • Cyclic GMP-Dependent Protein Kinases / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster
  • Growth Cones / metabolism
  • Ion Channels / genetics*
  • Ion Channels / metabolism
  • Mechanotransduction, Cellular / genetics
  • Mice
  • Mice, Knockout
  • Nerve Regeneration / genetics
  • Nitric Oxide Synthase / metabolism
  • Regeneration / genetics*
  • Sensory Receptor Cells / metabolism
  • Sensory Receptor Cells / physiology

Substances

  • Drosophila Proteins
  • Ion Channels
  • Piezo protein, Drosophila
  • Piezo1 protein, mouse
  • Nitric Oxide Synthase
  • Cyclic GMP-Dependent Protein Kinases
  • for protein, Drosophila
  • Calcium