Plasticity of the Electrical Connectome of C. elegans

Cell. 2019 Feb 21;176(5):1174-1189.e16. doi: 10.1016/j.cell.2018.12.024. Epub 2019 Jan 24.

Abstract

The specific patterns and functional properties of electrical synapses of a nervous system are defined by the neuron-specific complement of electrical synapse constituents. We systematically examined the molecular composition of the electrical connectome of the nematode C. elegans through a genome- and nervous-system-wide analysis of the expression patterns of the invertebrate electrical synapse constituents, the innexins. We observe highly complex combinatorial expression patterns throughout the nervous system and found that these patterns change in a strikingly neuron-type-specific manner throughout the nervous system when animals enter an insulin-controlled diapause arrest stage under harsh environmental conditions, the dauer stage. By analyzing several individual synapses, we demonstrate that dauer-specific electrical synapse remodeling is responsible for specific aspects of the altered locomotory and chemosensory behavior of dauers. We describe an intersectional gene regulatory mechanism involving terminal selector and FoxO transcription factors mediating dynamic innexin expression plasticity in a neuron-type- and environment-specific manner.

Keywords: Caenorhabditis elegans; connectome; electrical synapse; innexins; synaptic plasticity.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / metabolism
  • Connectome / methods
  • Electrical Synapses / metabolism*
  • Gene Expression Regulation, Developmental / genetics
  • Larva / metabolism
  • Neuronal Plasticity / physiology*
  • Neurons / metabolism
  • Signal Transduction
  • Synapses / metabolism
  • Transcription Factors / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Transcription Factors