Wengen, the Sole Tumour Necrosis Factor Receptor in Drosophila, Collaborates with Moesin to Control Photoreceptor Axon Targeting during Development

Wenjing Ruan,Edward A Fon,Philip A Barker,Julie Desbarats,Nicolas Unsain,Andreas Bergmann

doi:10.1371/journal.pone.0060091

Wenjing Ruan, Edward A Fon + Show 4 more

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https://doi.org/10.1371/journal.pone.0060091

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Abstract

Photoreceptor neurons (R cells) in the Drosophila eye define a map of visual space by connecting to targets in distinct layers of the optic lobe, with R1-6 cells connecting to the lamina (the first optic ganglion) and R7 and R8 cells connecting to the medulla (the second optic ganglion). Here, we show that Wengen (Wgn) directly binds Moesin (Moe) through a cytosolic membrane proximal domain and this interaction is important for mediating two distinct aspects of axonal targeting. First, we show that loss of wgn or moe function disrupts cell autonomous R8 axon targeting. Second, we report that wgn or moe mutants show defects in R2–R5 targeting that result from disruption of non-cell autonomous effects, which are secondary to the cell autonomous R8 phenotype. Thus, these studies reveal that the Wgn-Moe signaling cascade plays a key role in photoreceptor target field innervations through cell autonomous and non-cell autonomous mechanisms.

Highlights

Determining the molecular basis of neuronal targeting and identifying the mechanisms that lead to the establishment of synaptic circuits is a critical issue in neurobiology
24B10 to visualize all R cell axons. (D–F) Samples were labeled with Ro-tau-LacZ marker and stained by anti-beta galactosidase to visualize R2–R5 axons. (A9–C9) Magnified view of medullar areas in axonal targeting defects. (A–C). (A) In wild-type flies, R1-6 growth cones terminated in the lamina to form the lamina plexus, while R7 and R8 axons projected into the medulla
R1-6 axons normally project towards the posterior aspect of the eye imaginal disc, pass through the optic stalk, fan out and terminate in the first optic ganglion, where they form the lamina plexus [3,4]

Summary

Introduction

Determining the molecular basis of neuronal targeting and identifying the mechanisms that lead to the establishment of synaptic circuits is a critical issue in neurobiology. Neurons develop and extend processes in a stepwise and stereotypical fashion and it is certain that short- and long-range guidance cues can attract or repel growth cones, and facilitate or inhibit synapse formation [1,2]. Our knowledge of the specific mechanisms that allow developing neurons to seek out appropriate target zones and form synapses remains incomplete. The R8 photoreceptor differentiates earliest and is the first to extend its axon into the optic lobe, followed by R1-6 and R7. The R1-6 growth cones follow R8 axons only to the lamina where they terminate. R7 growth cones follow R8 axons through the lamina and into the medulla and terminate into a deeper layer (M6)

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