Deconstruction of the Beaten Path-Sidestep interaction network provides insights into neuromuscular system development

  1. Hanqing Li
  2. Ash Watson
  3. Agnieszka Olechwier
  4. Michael Anaya
  5. Siamak K Sorooshyari
  6. Dermott P Harnett
  7. Hyung-Kook (Peter) Lee
  8. Jost Vielmetter
  9. Mario A Fares
  10. K Christopher Garcia
  11. Engin Özkan
  12. Juan-Pablo Labrador
  13. Kai Zinn  Is a corresponding author
  1. California Institute of Technology, United States
  2. Trinity College Dublin, Ireland
  3. University of Chicago, United States
  4. Ellipsis Health, United States
  5. Howard Hughes Medical Institute, Stanford University School of Medicine, United States

Abstract

An "interactome" screen of all Drosophila cell-surface and secreted proteins containing immunoglobulin superfamily (IgSF) domains discovered a network formed by paralogs of Beaten Path (Beat) and Sidestep (Side), a ligand-receptor pair that is central to motor axon guidance. Here we describe a new method for interactome screening, the Bio-Plex Interactome Assay (BPIA), which allows identification of many interactions in a single sample. Using the BPIA, we "deorphanized" four more members of the Beat-Side network. We confirmed interactions using surface plasmon resonance. The expression patterns of beat and side genes suggest that Beats are neuronal receptors for Sides expressed on peripheral tissues. side-VI is expressed in muscle fibers targeted by the ISNb nerve, as well as at growth cone choice points and synaptic targets for the ISN and TN nerves. beat-V genes, encoding Side-VI receptors, are expressed in ISNb and ISN motor neurons.

Article and author information

Author details

  1. Hanqing Li

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ash Watson

    Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  3. Agnieszka Olechwier

    Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Michael Anaya

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Siamak K Sorooshyari

    Ellipsis Health, San Francisco, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1172-6291
  6. Dermott P Harnett

    Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  7. Hyung-Kook (Peter) Lee

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jost Vielmetter

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Mario A Fares

    Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  10. K Christopher Garcia

    Department of Molecular and Cellular Physiology, Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9273-0278
  11. Engin Özkan

    Department of Biochemistry and Molecular 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:" 0000-0002-0263-6729
  12. Juan-Pablo Labrador

    Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland
    Competing interests
    The authors declare that no competing interests exist.
  13. Kai Zinn

    Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, United States
    For correspondence
    zinnk@caltech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6706-5605

Funding

NIH (R37)

  • Kai Zinn

SFI

  • Juan-Pablo Labrador

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

Reviewing Editor

  1. Graeme W Davis, University of California, San Francisco, United States

Version history

  1. Received: April 27, 2017
  2. Accepted: July 28, 2017
  3. Accepted Manuscript published: August 15, 2017 (version 1)
  4. Accepted Manuscript updated: August 15, 2017 (version 2)
  5. Version of Record published: August 31, 2017 (version 3)

Copyright

© 2017, Li 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. Hanqing Li
  2. Ash Watson
  3. Agnieszka Olechwier
  4. Michael Anaya
  5. Siamak K Sorooshyari
  6. Dermott P Harnett
  7. Hyung-Kook (Peter) Lee
  8. Jost Vielmetter
  9. Mario A Fares
  10. K Christopher Garcia
  11. Engin Özkan
  12. Juan-Pablo Labrador
  13. Kai Zinn
(2017)
Deconstruction of the Beaten Path-Sidestep interaction network provides insights into neuromuscular system development
eLife 6:e28111.
https://doi.org/10.7554/eLife.28111

Share this article

https://doi.org/10.7554/eLife.28111

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