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Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system

Nature Neuroscience volume 14, pages 314–323 (2011)Cite this article

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Abstract

Neuronal connections are often organized in layers that contain synapses between neurons that have similar functions. In Drosophila, R7 and R8 photoreceptors, which detect different wavelengths, form synapses in distinct medulla layers. The mechanisms underlying the specificity of synaptic-layer selection remain unclear. We found that Golden Goal (Gogo) and Flamingo (Fmi), two cell-surface proteins involved in photoreceptor targeting, functionally interact in R8 photoreceptor axons. Our results indicate that Gogo promotes R8 photoreceptor axon adhesion to the temporary layer M1, whereas Gogo and Fmi collaborate to mediate axon targeting to the final layer M3. Structure-function analysis suggested that Gogo and Fmi interact with intracellular components through the Gogo cytoplasmic domain. Moreover, Fmi was also required in target cells for R8 photoreceptor axon targeting. We propose that Gogo acts as a functional partner of Fmi for R8 photoreceptor axon targeting and that the dynamic regulation of their interaction specifies synaptic-layer selection of photoreceptors.

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Figure 1: fmi regulates synaptic-layer targeting and does not require its cytoplasmic domain.
Figure 2: Phenotypic similarities between gogo and fmi.
Figure 3: gogo genetically interacts with fmi.
Figure 4: Gogo and Fmi colocalize at cell-cell contacts.
Figure 5: Gogo interacts with Fmi in cis in wing cells.
Figure 6: Gogo and Fmi interact with intracellular components through the Gogo cytoplasmic domain.
Figure 7: Fmi is required in target cells for R8 photoreceptor synaptic-layer targeting.
Figure 8: Antagonistic interaction between Gogo and Fmi at the M1 layer.

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Acknowledgements

We thank N. Hengrung for helping with BiFC experiments, I. Siwanowicz for helping with agarose sections and M. Braun for electron microscopy sections. We thank I. Salecker, T. Clandinin, J. Axelrod, D. Strutt, B. Dickson, K. Keleman, H. Oda, H. Bellen, J. Morante, J. Smith, Developmental Studies Hybridoma Bank (University of Iowa), Drosophila Genetic Resource Center (Kyoto), Exelixis Collection at Harvard and Bloomington Stock Center for reagents, and FlyBase for information resources. We thank R. Klein, F. Schnorrer, J. Egea for suggestions and comments, and members of the Suzuki laboratory for critical discussions. This work was supported by the Max Planck Society and an individual grant from the Deutsche Forschungsgemeinschaft (T.S.).

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Author notes

  1. Satoko Hakeda-Suzuki and Sandra Berger-Müller: These authors contributed equally to this work.

Authors and Affiliations

  1. Max Planck Institute of Neurobiology, Martinsried, Germany

    Satoko Hakeda-Suzuki, Sandra Berger-Müller, Tatiana Tomasi & Takashi Suzuki

  2. Graduate School of Biostudies, Kyoto University, Kyoto, Japan

    Tadao Usui, Shin-ya Horiuchi & Tadashi Uemura

  3. Japan Science and Technology Agency, CREST, Kyoto, Japan

    Tadashi Uemura

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Contributions

S.H.-S. conducted the genetic and histological experiments. S.B.-M. conducted the cell culture and biochemical experiments and assisted with the genetic experiments. T.T. conducted the lamina cartridge experiments. T. Usui, S.-y.H. and T. Uemura generated and provided the hypomorphic allele of fmi. S.H.-S. and T.S. designed the experiments. S.B.-M., S.H.-S. and T.S. wrote the paper.

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Correspondence to Takashi Suzuki.

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Hakeda-Suzuki, S., Berger-Müller, S., Tomasi, T. et al. Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system. Nat Neurosci 14, 314–323 (2011). https://doi.org/10.1038/nn.2756

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