Prenylation of Axonally Translated Rac1 Controls NGF-Dependent Axon Growth

Dev Cell. 2020 Jun 22;53(6):691-705.e7. doi: 10.1016/j.devcel.2020.05.020. Epub 2020 Jun 12.

Abstract

Compartmentalized signaling is critical for cellular organization and specificity of functional outcomes in neurons. Here, we report that post-translational lipidation of newly synthesized proteins in axonal compartments allows for short-term and autonomous responses to extrinsic cues. Using conditional mutant mice, we found that protein prenylation is essential for sympathetic axon innervation of target organs. We identify a localized requirement for prenylation in sympathetic axons to promote axonal growth in response to the neurotrophin, nerve growth factor (NGF). NGF triggers prenylation of proteins including the Rac1 GTPase in axons, counter to the canonical view of prenylation as constitutive, and strikingly, in a manner dependent on axonal protein synthesis. Newly prenylated proteins localize to TrkA-harboring endosomes in axons and promote receptor trafficking necessary for axonal growth. Thus, coupling of prenylation to local protein synthesis presents a mechanism for spatially segregated cellular functions during neuronal development.

Keywords: compartmentalized signaling; local translation; neuronal development; neurotrophin trafficking; protein lipidation.

Publication types

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

MeSH terms

  • Animals
  • Axon Guidance*
  • Axons / metabolism*
  • Cells, Cultured
  • Endosomes / metabolism
  • HEK293 Cells
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Nerve Growth Factor / metabolism*
  • Neuropeptides / genetics
  • Neuropeptides / metabolism*
  • PC12 Cells
  • Protein Prenylation*
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, trkA / metabolism
  • rac1 GTP-Binding Protein / genetics
  • rac1 GTP-Binding Protein / metabolism*

Substances

  • Neuropeptides
  • Rac1 protein, mouse
  • Nerve Growth Factor
  • Receptor, trkA
  • rac1 GTP-Binding Protein