Temporal transcription factors determine circuit membership by permanently altering motor neuron-to-muscle synaptic partnerships

Elife. 2020 May 11:9:e56898. doi: 10.7554/eLife.56898.

Abstract

How circuit wiring is specified is a key question in developmental neurobiology. Previously, using the Drosophila motor system as a model, we found the classic temporal transcription factor Hunchback acts in NB7-1 neuronal stem cells to control the number of NB7-1 neuronal progeny form functional synapses on dorsal muscles (Meng et al., 2019). However, it is unknown to what extent control of motor neuron-to-muscle synaptic partnerships is a general feature of temporal transcription factors. Here, we perform additional temporal transcription factor manipulations-prolonging expression of Hunchback in NB3-1, as well as precociously expressing Pdm and Castor in NB7-1. We use confocal microscopy, calcium imaging, and electrophysiology to show that in every manipulation there are permanent alterations in neuromuscular synaptic partnerships. Our data show temporal transcription factors, as a group of molecules, are potent determinants of synaptic partner choice and therefore ultimately control circuit membership.

Keywords: D. melanogaster; developmental biology; motor neuron; neuronal stem cell; neuroscience; transcription factors.

Publication types

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

MeSH terms

  • Animals
  • Cell Lineage
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster
  • Gene Expression Regulation, Developmental
  • Genes, Insect
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Motor Neurons / physiology*
  • Muscles / physiology
  • Neuromuscular Junction / physiology*
  • POU Domain Factors / genetics
  • POU Domain Factors / metabolism*
  • Stem Cells
  • Synapses / physiology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • Homeodomain Proteins
  • POU Domain Factors
  • Transcription Factors
  • cas protein, Drosophila
  • hb protein, Drosophila
  • pdm2 protein, Drosophila