Abstract
Transmembrane protein Golden goal (Gogo) interacts with atypical cadherin Flamingo (Fmi) 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 shapes the entire organization of the visual system.
Highlights
36 37 During development, well-defined synaptic connections are formed in the brain between specific neurons to facilitate higher-order information processing
These results indicate that the glial insulin signal controls Gogo phosphorylation, thereby regulating growth cone dynamics, including the formation of the horseshoe shape and filopodia extension
The results indicate that Fmi alone promotes vertical filopodia elongation into the M3 layer during phase 3. 137 Gogo and Fmi Cooperatively Guide R8 Axons to Encircle the Columnar Center of the 138 Medulla R8 cell-specific strong loss-of function (LOF) animals were generated to observe phase-specific Gogo and Fmi functions (Figure 2)
Summary
21 22 Transmembrane protein Golden goal (Gogo) interacts with atypical cadherin Flamingo to direct R8 photoreceptor axons in the Drosophila visual system. The Drosophila visual system is an attractive model for studying the formation of the functional organization of synaptic connections because its optic ganglion has a layered and columnar structure (Hadjieconomou et al, 2011; Millard and Pecot, 2018; Sanes and Zipursky, 2010). In phase 3, R8 axons only expressed Fmi, which directed them to the M3 layer (no gogo function) These results indicate that the glial insulin signal controls Gogo phosphorylation, thereby regulating growth cone dynamics, including the formation of the horseshoe shape and filopodia extension. Overall, this regulates axon–column and axon–axon interactions. This mechanism maintains the regular distance between R8 axons and enables the ordered R8 axonal targeting of the column
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