Hydrogen peroxide is a neuronal alarmin that triggers specific RNAs, local translation of Annexin A2, and cytoskeletal remodeling in Schwann cells

RNA. 2018 Jul;24(7):915-925. doi: 10.1261/rna.064816.117. Epub 2018 Apr 11.

Abstract

Schwann cells are key players in neuro-regeneration: They sense "alarm" signals released by degenerating nerve terminals and differentiate toward a proregenerative phenotype, with phagocytosis of nerve debris and nerve guidance. At the murine neuromuscular junction, hydrogen peroxide (H2O2) is a key signal of Schwann cells' activation in response to a variety of nerve injuries. Here we report that Schwann cells exposed to low doses of H2O2 rewire the expression of several RNAs at both transcriptional and translational levels. Among the genes positively regulated at both levels, we identified an enriched cluster involved in cytoskeleton remodeling and cell migration, with the Annexin (Anxa) proteins being the most represented family. We show that both Annexin A2 (Anxa2) transcript and protein accumulate at the tips of long pseudopods that Schwann cells extend upon H2O2 exposure. Interestingly, Schwann cells reply to this signal and to nerve injury by locally translating Anxa2 in pseudopods, and undergo an extensive cytoskeleton remodeling. Our results show that, similarly to neurons, Schwann cells take advantage of local protein synthesis to change shape and move toward damaged axonal terminals to facilitate axonal regeneration.

Keywords: Annexin A2; RNA transport; Schwann cells; axonal regeneration; hydrogen peroxide; local protein synthesis; local translation; neuromuscular junction; next-generation sequencing; polysome profiling; translatome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Annexin A2 / biosynthesis*
  • Annexin A2 / genetics
  • Annexin A2 / metabolism
  • Cells, Cultured
  • Cytoskeleton / ultrastructure
  • Gene Expression Regulation / drug effects
  • Hydrogen Peroxide / pharmacology*
  • Mice, Inbred C57BL
  • Nerve Degeneration / metabolism
  • Nerve Degeneration / physiopathology
  • Protein Biosynthesis
  • RNA / biosynthesis
  • Schwann Cells / cytology
  • Schwann Cells / drug effects
  • Schwann Cells / metabolism*
  • Schwann Cells / ultrastructure
  • Transcriptome / drug effects

Substances

  • Annexin A2
  • RNA
  • Hydrogen Peroxide