Sarcomeres Pattern Proprioceptive Sensory Dendritic Endings through UNC-52/Perlecan in C. elegans

Dev Cell. 2015 May 26;33(4):388-400. doi: 10.1016/j.devcel.2015.03.010. Epub 2015 May 14.

Abstract

Sensory dendrites innervate peripheral tissues through cell-cell interactions that are poorly understood. The proprioceptive neuron PVD in C. elegans extends regular terminal dendritic branches between muscle and hypodermis. We found that the PVD branch pattern was instructed by adhesion molecule SAX-7/L1CAM, which formed regularly spaced stripes on the hypodermal cell. The regularity of the SAX-7 pattern originated from the repeated and regularly spaced dense body of the sarcomeres in the muscle. The extracellular proteoglycan UNC-52/Perlecan linked the dense body to the hemidesmosome on the hypodermal cells, which in turn instructed the SAX-7 stripes and PVD dendrites. Both UNC-52 and hemidesmosome components exhibited highly regular stripes that interdigitated with the SAX-7 stripe and PVD dendrites, reflecting the striking precision of subcellular patterning between muscle, hypodermis, and dendrites. Hence, the muscular contractile apparatus provides the instructive cues to pattern proprioceptive dendrites.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Caenorhabditis elegans Proteins / metabolism*
  • Dendrites / metabolism*
  • Fluorescent Antibody Technique
  • Heparan Sulfate Proteoglycans / metabolism*
  • Image Processing, Computer-Assisted
  • Membrane Proteins / metabolism*
  • Microscopy, Confocal
  • Muscles / cytology
  • Muscles / metabolism*
  • Neural Cell Adhesion Molecule L1 / metabolism
  • Neural Cell Adhesion Molecules / metabolism
  • Neurons / cytology
  • Neurons / metabolism
  • Proteoglycans / metabolism*
  • Sarcomeres / metabolism*
  • Subcellular Fractions
  • Subcutaneous Tissue / metabolism*

Substances

  • Caenorhabditis elegans Proteins
  • Heparan Sulfate Proteoglycans
  • Membrane Proteins
  • Neural Cell Adhesion Molecule L1
  • Neural Cell Adhesion Molecules
  • Proteoglycans
  • SAX-7 protein, C elegans
  • unc-52 protein, C elegans
  • perlecan