1. Developmental Biology
  2. Neuroscience

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

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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.

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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Further reading

    1. Cell Biology
    2. Neuroscience

    Transsynaptic interactions between IgSF proteins DIP-α and Dpr10 are required for motor neuron targeting specificity

    James Ashley, Violet Sorrentino ... Robert A Carrillo
    Research Article Updated

    The Drosophila larval neuromuscular system provides an ideal context in which to study synaptic partner choice, because it contains a small number of pre- and postsynaptic cells connected in an invariant pattern. The discovery of interactions between two subfamilies of IgSF cell surface proteins, the Dprs and the DIPs, provided new candidates for cellular labels controlling synaptic specificity. Here we show that DIP-α is expressed by two identified motor neurons, while its binding partner Dpr10 is expressed by postsynaptic muscle targets. Removal of either DIP-α or Dpr10 results in loss of specific axonal branches and NMJs formed by one motor neuron, MNISN-1s, while other branches of the MNISN-1s axon develop normally. The temporal and spatial expression pattern of dpr10 correlates with muscle innervation by MNISN-1s during embryonic development. We propose a model whereby DIP-α and Dpr10 on opposing synaptic partners interact with each other to generate proper motor neuron connectivity.