Prd1 associates with the clathrin adaptor α-Adaptin and the kinesin-3 Imac/Unc-104 to govern dendrite pruning in Drosophila

PLoS Biol. 2018 Aug 24;16(8):e2004506. doi: 10.1371/journal.pbio.2004506. eCollection 2018 Aug.

Abstract

Refinement of the nervous system depends on selective removal of excessive axons/dendrites, a process known as pruning. Drosophila ddaC sensory neurons prune their larval dendrites via endo-lysosomal degradation of the L1-type cell adhesion molecule (L1-CAM), Neuroglian (Nrg). Here, we have identified a novel gene, pruning defect 1 (prd1), which governs dendrite pruning of ddaC neurons. We show that Prd1 colocalizes with the clathrin adaptor protein α-Adaptin (α-Ada) and the kinesin-3 immaculate connections (Imac)/Uncoordinated-104 (Unc-104) in dendrites. Moreover, Prd1 physically associates with α-Ada and Imac, which are both critical for dendrite pruning. Prd1, α-Ada, and Imac promote dendrite pruning via the regulation of endo-lysosomal degradation of Nrg. Importantly, genetic interactions among prd1, α-adaptin, and imac indicate that they act in the same pathway to promote dendrite pruning. Our findings indicate that Prd1, α-Ada, and Imac act together to regulate discrete distribution of α-Ada/clathrin puncta, facilitate endo-lysosomal degradation, and thereby promote dendrite pruning in sensory neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Protein Complex alpha Subunits / genetics*
  • Adaptor Protein Complex alpha Subunits / metabolism
  • Animals
  • Brain / cytology
  • Brain / metabolism
  • Cell Adhesion Molecules, Neuronal / genetics*
  • Cell Adhesion Molecules, Neuronal / metabolism
  • Dendrites / metabolism*
  • Dendrites / ultrastructure
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / metabolism
  • Endosomes / metabolism
  • Endosomes / ultrastructure
  • Gene Expression Regulation, Developmental
  • Kinesins / genetics*
  • Kinesins / metabolism
  • Larva / genetics
  • Larva / growth & development
  • Larva / metabolism
  • Lysosomes / metabolism
  • Lysosomes / ultrastructure
  • Metamorphosis, Biological / genetics
  • Neural Cell Adhesion Molecule L1 / genetics*
  • Neural Cell Adhesion Molecule L1 / metabolism
  • Neuronal Plasticity / genetics*
  • Protein Binding
  • Proteolysis
  • Sensory Receptor Cells / cytology
  • Sensory Receptor Cells / metabolism
  • Signal Transduction

Substances

  • Adaptor Protein Complex alpha Subunits
  • Cell Adhesion Molecules, Neuronal
  • Drosophila Proteins
  • Neural Cell Adhesion Molecule L1
  • Nrg protein, Drosophila
  • Unc-104 protein, Drosophila
  • Kinesins

Grants and funding

Temasek Life Sciences Laboratory, Singapore (grant number TLL-2040). Received by FY. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.