Stereotyped terminal axon branching of leg motor neurons mediated by IgSF proteins DIP-α and Dpr10

  1. Lalanti Venkatasubramanian
  2. Zhenhao Guo
  3. Shuwa Xu
  4. Liming Tan
  5. Qi Xiao
  6. Sonal Nagarkar-Jaiswal
  7. Richard S Mann  Is a corresponding author
  1. Columbia University, United States
  2. University of California, Los Angeles, United States
  3. Baylor College of Medicine, United States

Abstract

For animals to perform coordinated movements requires the precise organization of neural circuits controlling motor function. Motor neurons (MNs), key components of these circuits, project their axons from the central nervous system and form precise terminal branching patterns at specific muscles. Focusing on the Drosophila leg neuromuscular system we show that the stereotyped terminal branching of a subset of MNs is mediated by interacting transmembrane Ig superfamily proteins DIP-α and Dpr10, present in MNs and target muscles, respectively. The DIP-α/Dpr10 interaction is needed only after MN axons reach the vicinity of their muscle targets. Live imaging suggests that precise terminal branching patterns are gradually established by DIP-α/Dpr10-dependent interactions between fine axon filopodia and developing muscles. Further, different leg MNs depend on the DIP-α and Dpr10 interaction to varying degrees that correlate with the morphological complexity of the MNs and their muscle targets.

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All data generated or analysed during this study are included in the manuscript and supporting files

Article and author information

Author details

  1. Lalanti Venkatasubramanian

    Department of Biochemistry and Molecular Biophysics, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Zhenhao Guo

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shuwa Xu

    Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Liming Tan

    Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Qi Xiao

    Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Sonal Nagarkar-Jaiswal

    Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Richard S Mann

    Department of Biochemistry and Molecular Biophysics, Columbia University, New York, United States
    For correspondence
    rsm10@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4749-2765

Funding

National Institutes of Health (R01NS070644)

  • Richard S Mann

National Institutes of Health (U19NS104655)

  • Richard S Mann

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Version history

  1. Received: October 9, 2018
  2. Accepted: January 31, 2019
  3. Accepted Manuscript published: February 4, 2019 (version 1)
  4. Version of Record published: February 26, 2019 (version 2)

Copyright

© 2019, Venkatasubramanian 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. Lalanti Venkatasubramanian
  2. Zhenhao Guo
  3. Shuwa Xu
  4. Liming Tan
  5. Qi Xiao
  6. Sonal Nagarkar-Jaiswal
  7. Richard S Mann
(2019)
Stereotyped terminal axon branching of leg motor neurons mediated by IgSF proteins DIP-α and Dpr10
eLife 8:e42692.
https://doi.org/10.7554/eLife.42692

Share this article

https://doi.org/10.7554/eLife.42692

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