MicroRNAs in the axon locally mediate the effects of chondroitin sulfate proteoglycans and cGMP on axonal growth

Dev Neurobiol. 2015 Dec;75(12):1402-19. doi: 10.1002/dneu.22292. Epub 2015 Jun 24.

Abstract

Axonal miRNAs locally regulate axonal growth by modulating local protein composition. Whether localized miRNAs in the axon mediate the inhibitory effect of Chondroitin sulfate proteoglycans (CSPGs) on the axon remains unknown. We showed that in cultured cortical neurons, axonal application of CSPGs inhibited axonal growth and altered axonal miRNA profiles, whereas elevation of axonal cyclic guanosine monophosphate (cGMP) levels by axonal application of sildenafil reversed the effect of CSPGs on inhibition of axonal growth and on miRNA profiles. Specifically, CSPGs elevated and reduced axonal levels of miR-29c and integrin β1 (ITGB1) proteins, respectively, while elevation of cGMP levels overcame these CSPG effects. Gain-of- and loss-of-function experiments demonstrated that miR-29c in the distal axon mediates axonal growth downstream of CSPGs and cGMP by regulating axonal protein levels of ITGB1, FAK, and RhoA. Together, our data demonstrate that axonal miRNAs play an important role in mediating the inhibitory action of CSPGs on axonal growth and that miR-29c at least partially mediates this process.

Keywords: axon growth; cGMP; chondroitin sulfate proteoglycans; miRNA.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Axons / drug effects
  • Axons / physiology*
  • Cell Enlargement / drug effects
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / physiology
  • Chondroitin Sulfate Proteoglycans / metabolism*
  • Cyclic GMP / metabolism*
  • Cyclic Nucleotide Phosphodiesterases, Type 5 / metabolism
  • Focal Adhesion Kinase 1 / metabolism
  • HEK293 Cells
  • Humans
  • MicroRNAs / metabolism*
  • Phosphodiesterase 5 Inhibitors / pharmacology
  • RNA, Messenger / metabolism
  • Rats, Wistar
  • Sildenafil Citrate / pharmacology

Substances

  • Chondroitin Sulfate Proteoglycans
  • MicroRNAs
  • Phosphodiesterase 5 Inhibitors
  • RNA, Messenger
  • Sildenafil Citrate
  • Focal Adhesion Kinase 1
  • Ptk2 protein, rat
  • Cyclic Nucleotide Phosphodiesterases, Type 5
  • Cyclic GMP