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

  1. Julia L Meng
  2. Yupu Wang
  3. Robert A Carrillo
  4. Ellie Heckscher  Is a corresponding author
  1. University of Chicago, United States

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 how many 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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1, 1S2, 3, 4, 5.

Article and author information

Author details

  1. Julia L Meng

    Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Yupu Wang

    Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Robert A Carrillo

    Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2067-9861
  4. Ellie Heckscher

    Molecular Genetics and Cell Biology, University of Chicago, Chicago, United States
    For correspondence
    heckscher@uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7618-0616

Funding

National Institute of Neurological Disorders and Stroke (R01-NS105748)

  • Ellie Heckscher

National Institute of General Medical Sciences (T32 GM007183)

  • Julia L Meng

National Science Foundation ((DGE-1746045))

  • Julia L Meng

National Institute of Neurological Disorders and Stroke (K01 NS102342)

  • Robert A Carrillo

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Oliver Hobert, Howard Hughes Medical Institute, Columbia University, United States

Version history

  1. Received: March 15, 2020
  2. Accepted: May 9, 2020
  3. Accepted Manuscript published: May 11, 2020 (version 1)
  4. Version of Record published: May 21, 2020 (version 2)

Copyright

© 2020, Meng et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Julia L Meng
  2. Yupu Wang
  3. Robert A Carrillo
  4. Ellie Heckscher
(2020)
Temporal transcription factors determine circuit membership by permanently altering motor neuron-to-muscle synaptic partnerships
eLife 9:e56898.
https://doi.org/10.7554/eLife.56898

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https://doi.org/10.7554/eLife.56898