Glial insulin regulates cooperative or antagonistic Golden goal/Flamingo interactions during photoreceptor axon guidance
- Tokyo Institute of Technology, Japan
- Niigata University, Niigata, Japan
- 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
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
- Claude Desplan, New York University, United States
Version history
- Received: January 20, 2021
- Accepted: March 2, 2021
- Accepted Manuscript published: March 5, 2021 (version 1)
- 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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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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