Activation of the unfolded protein response promotes axonal regeneration after peripheral nerve injury

Sci Rep. 2016 Feb 24:6:21709. doi: 10.1038/srep21709.

Abstract

Although protein-folding stress at the endoplasmic reticulum (ER) is emerging as a driver of neuronal dysfunction in models of spinal cord injury and neurodegeneration, the contribution of this pathway to peripheral nerve damage remains poorly explored. Here we targeted the unfolded protein response (UPR), an adaptive reaction against ER stress, in mouse models of sciatic nerve injury and found that ablation of the transcription factor XBP1, but not ATF4, significantly delay locomotor recovery. XBP1 deficiency led to decreased macrophage recruitment, a reduction in myelin removal and axonal regeneration. Conversely, overexpression of XBP1s in the nervous system in transgenic mice enhanced locomotor recovery after sciatic nerve crush, associated to an improvement in key pro-regenerative events. To assess the therapeutic potential of UPR manipulation to axonal regeneration, we locally delivered XBP1s or an shRNA targeting this transcription factor to sensory neurons of the dorsal root ganglia using a gene therapy approach and found an enhancement or reduction of axonal regeneration in vivo, respectively. Our results demonstrate a functional role of specific components of the ER proteostasis network in the cellular changes associated to regeneration and functional recovery after peripheral nerve injury.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Activating Transcription Factor 4 / metabolism
  • Animals
  • Axons / physiology
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Endoplasmic Reticulum Stress
  • Gene Expression
  • Locomotion
  • Macrophages / physiology
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Regeneration*
  • Peripheral Nerve Injuries / physiopathology*
  • Recovery of Function
  • Sciatic Nerve / injuries
  • Sciatic Nerve / metabolism
  • Sciatic Nerve / physiopathology*
  • Unfolded Protein Response*
  • X-Box Binding Protein 1 / genetics
  • X-Box Binding Protein 1 / metabolism

Substances

  • ATF4 protein, human
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • X-Box Binding Protein 1
  • Xbp1 protein, mouse
  • Activating Transcription Factor 4