Adhesive L1CAM-Robo Signaling Aligns Growth Cone F-Actin Dynamics to Promote Axon-Dendrite Fasciculation in C. elegans

Dev Cell. 2019 Jan 28;48(2):215-228.e5. doi: 10.1016/j.devcel.2018.10.028. Epub 2018 Dec 13.

Abstract

Neurite fasciculation through contact-dependent signaling is important for the wiring and function of the neuronal circuits. Here, we describe a type of axon-dendrite fasciculation in C. elegans, where proximal dendrites of the nociceptor PVD adhere to the axon of the ALA interneuron. This axon-dendrite fasciculation is mediated by a previously uncharacterized adhesive signaling by the ALA membrane signal SAX-7/L1CAM and the PVD receptor SAX-3/Robo but independent of Slit. L1CAM physically interacts with Robo and instructs dendrite adhesion in a Robo-dependent manner. Fasciculation mediated by L1CAM-Robo signaling aligns F-actin dynamics in the dendrite growth cone and facilitates dynamic growth cone behaviors for efficient dendrite guidance. Disruption of PVD dendrite fasciculation impairs nociceptive mechanosensation and rhythmicity in body curvature, suggesting that dendrite fasciculation governs the functions of mechanosensory circuits. Our work elucidates the molecular mechanisms by which adhesive axon-dendrite signaling shapes the construction and function of sensory neuronal circuits.

Keywords: C. elegans; F-actin; Robo; axon; cell adhesion molecule; cytoskeleton; dendrite; fasciculation; growth cone; somatosensation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism*
  • Actins / metabolism
  • Animals
  • Axon Fasciculation / physiology*
  • Axons / metabolism
  • Caenorhabditis elegans / growth & development
  • Caenorhabditis elegans Proteins
  • Cytoskeleton / metabolism
  • Dendrites / physiology
  • Growth Cones / metabolism*
  • Nerve Tissue Proteins / metabolism
  • Neural Cell Adhesion Molecule L1 / metabolism*
  • Receptors, Immunologic / metabolism
  • Roundabout Proteins

Substances

  • Actins
  • Caenorhabditis elegans Proteins
  • Nerve Tissue Proteins
  • Neural Cell Adhesion Molecule L1
  • Receptors, Immunologic