Glial insulin regulates cooperative or antagonistic Golden goal/Flamingo interactions during photoreceptor axon guidance

  1. Hiroki Takechi
  2. Satoko Hakeda-Suzuki  Is a corresponding author
  3. Yohei Nitta
  4. Yuichi Ishiwata
  5. Riku Iwanaga
  6. Makoto Sato
  7. Atsushi Sugie
  8. Takashi Suzuki  Is a corresponding author
  1. Tokyo Institute of Technology, Japan
  2. Niigata University, Niigata, Japan
  3. Kanazawa University, Japan

Abstract

Transmembrane protein Golden goal (Gogo) interacts with atypical cadherin Flamingo to direct R8 photoreceptor axons in the Drosophila visual system. However, the precise mechanisms underlying Gogo regulation during columnar- and layer-specific R8 axon targeting are unknown. Our studies demonstrated that the insulin secreted from surface and cortex glia switches the phosphorylation status of Gogo, thereby regulating its two distinct functions. Non-phosphorylated Gogo mediates the initial recognition of the glial protrusion in the center of the medulla column, whereas phosphorylated Gogo suppresses radial filopodia extension by counteracting Flamingo to maintain a one axon to one column ratio. Later, Gogo expression ceases during the midpupal stage, thus allowing R8 filopodia to extend vertically into the M3 layer. These results demonstrate that the long- and short-range signaling between the glia and R8 axon growth cones regulates growth cone dynamics in a stepwise manner, and thus shape the entire organization of the visual system.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided.

Article and author information

Author details

  1. Hiroki Takechi

    School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  2. Satoko Hakeda-Suzuki

    School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Japan
    For correspondence
    hakeda@bio.titech.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
  3. Yohei Nitta

    Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0712-428X
  4. Yuichi Ishiwata

    School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Riku Iwanaga

    School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Makoto Sato

    Institute for Frontier Science Initiative, Kanazawa University, Kanazawa, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7763-0751
  7. Atsushi Sugie

    Center for Transdisciplinary Research, Niigata University, Niigata, Niigata, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Takashi Suzuki

    School of Life Science and Technology, Tokyo Institute of Technology, Yokohama, Japan
    For correspondence
    suzukit@bio.titech.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9093-2562

Funding

Japan Society for the Promotion of Science (19J14499)

  • Hiroki Takechi

Ministry of Education, Culture, Sports, Science and Technology (17H05761)

  • Makoto Sato

Ministry of Education, Culture, Sports, Science and Technology (19H04771)

  • Makoto Sato

Takeda Science Foundation (Life Sciemce Research Grant)

  • Atsushi Sugie

Takeda Science Foundation (Visionary Research Grant)

  • Takashi Suzuki

Japan Society for the Promotion of Science (18J00367)

  • Yohei Nitta

Japan Society for the Promotion of Science (18K06250)

  • Satoko Hakeda-Suzuki

Japan Society for the Promotion of Science (18K14835)

  • Yohei Nitta

Japan Society for the Promotion of Science (17H03542)

  • Makoto Sato

Japan Society for the Promotion of Science (17H04983)

  • Atsushi Sugie

Japan Society for the Promotion of Science (19K22592)

  • Atsushi Sugie

Ministry of Education, Culture, Sports, Science and Technology (16H06457)

  • Takashi Suzuki

Ministry of Education, Culture, Sports, Science and Technology (17H05739)

  • Makoto Sato

The authors declare that there was no funding for this work.

Reviewing Editor

  1. Claude Desplan, New York University, United States

Publication history

  1. Received: January 20, 2021
  2. Accepted: March 2, 2021
  3. Accepted Manuscript published: March 5, 2021 (version 1)
  4. Version of Record published: March 22, 2021 (version 2)

Copyright

© 2021, Takechi 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. Hiroki Takechi
  2. Satoko Hakeda-Suzuki
  3. Yohei Nitta
  4. Yuichi Ishiwata
  5. Riku Iwanaga
  6. Makoto Sato
  7. Atsushi Sugie
  8. Takashi Suzuki
(2021)
Glial insulin regulates cooperative or antagonistic Golden goal/Flamingo interactions during photoreceptor axon guidance
eLife 10:e66718.
https://doi.org/10.7554/eLife.66718

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