Autoinhibition of a Neuronal Kinesin UNC-104/KIF1A Regulates the Size and Density of Synapses

Cell Rep. 2016 Aug 23;16(8):2129-2141. doi: 10.1016/j.celrep.2016.07.043. Epub 2016 Aug 11.

Abstract

Kinesin motor proteins transport intracellular cargoes throughout cells by hydrolyzing ATP and moving along microtubule tracks. Intramolecular autoinhibitory interactions have been shown for several kinesins in vitro; however, the physiological significance of autoinhibition remains poorly understood. Here, we identified four mutations in the stalk region and motor domain of the synaptic vesicle (SV) kinesin UNC-104/KIF1A that specifically disrupt autoinhibition. These mutations augment both microtubule and cargo vesicle binding in vitro. In vivo, these mutations cause excessive activation of UNC-104, leading to decreased synaptic density, smaller synapses, and ectopic localization of SVs in the dendrite. We also show that the SV-bound small GTPase ARL-8 activates UNC-104 by unlocking the autoinhibition. These results demonstrate that the autoinhibitory mechanism is used to regulate the distribution of transport cargoes and is important for synaptogenesis in vivo.

MeSH terms

  • Animals
  • Biological Transport
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans / ultrastructure
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Dendrites / metabolism
  • Dendrites / ultrastructure
  • GTP Phosphohydrolases / genetics
  • GTP Phosphohydrolases / metabolism*
  • Gene Expression
  • Microtubules / metabolism*
  • Microtubules / ultrastructure
  • Mutation
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Protein Binding
  • Protein Domains
  • Synaptic Transmission
  • Synaptic Vesicles / metabolism*
  • Synaptic Vesicles / ultrastructure

Substances

  • Caenorhabditis elegans Proteins
  • Nerve Tissue Proteins
  • UNC-104 protein, C elegans
  • GTP Phosphohydrolases
  • arl-8 protein, C elegans