Abstract
Despite the importance of dendritic targeting in neural circuit assembly, the mechanisms by which it is controlled still remain incompletely understood. We previously showed that in the developing Drosophila antennal lobe, the Wnt5 protein forms a gradient that directs the ~45˚ rotation of a cluster of projection neuron (PN) dendrites, including the adjacent DA1 and VA1d dendrites. We report here that the Van Gogh (Vang) transmembrane planar cell polarity (PCP) protein is required for the rotation of the DA1/VA1d dendritic pair. Cell type-specific rescue and mosaic analyses showed that Vang functions in the olfactory receptor neurons (ORNs), suggesting a codependence of ORN axonal and PN dendritic targeting. Loss of Vang suppressed the repulsion of the VA1d dendrites by Wnt5, indicating that Wnt5 signals through Vang to direct the rotation of the DA1 and VA1d glomeruli. We observed that the Derailed (Drl)/Ryk atypical receptor tyrosine kinase is also required for the rotation of the DA1/VA1d dendritic pair. Antibody staining showed that Drl/Ryk is much more highly expressed by the DA1 dendrites than the adjacent VA1d dendrites. Mosaic and epistatic analyses showed that Drl/Ryk specifically functions in the DA1 dendrites in which it antagonizes the Wnt5-Vang repulsion and mediates the migration of the DA1 glomerulus towards Wnt5. Thus, the nascent DA1 and VA1d glomeruli appear to exhibit Drl/Ryk-dependent biphasic responses to Wnt5. Our work shows that the final patterning of the fly olfactory map is the result of an interplay between ORN axons and PN dendrites, wherein converging pre- and postsynaptic processes contribute key Wnt5 signaling components, allowing Wnt5 to orient the rotation of nascent synapses through a PCP mechanism.
Highlights
The prevailing view of neural circuit assembly is that axons and dendrites are separately guided by molecular gradients to their respective positions whereupon they form synapses with each other [1,2,3,4]
We demonstrate that the converging axons and dendrites contribute different signaling components to the Wnt5 pathway, the Van Gogh (Vang) Gogh and Derailed transmembrane receptors respectively, which allow Wnt5 to coordinately guide the targeting of the neurites
To elucidate the molecular mechanisms by which Wnt5 controls the rotation of the projection neuron (PN) dendrites, we screened a panel of signal transduction mutants for similar defects in DA1/VA1d rotation
Summary
The prevailing view of neural circuit assembly is that axons and dendrites are separately guided by molecular gradients to their respective positions whereupon they form synapses with each other [1,2,3,4]. Dendrites of 50 classes of uniglomerular projection neurons (PNs) form synapses with the axons of 50 classes of olfactory receptor neurons (ORNs) in the antennal lobe (AL) in unique glomeruli [6, 7] This precise glomerular map is thought to be established during the pupal stage by the targeting of PN dendrites [8,9,10]. We previously reported that during the establishment of the fly olfactory map, two adjacent dendritic arbors located at the dorsolateral region of the AL, the DA1 and VA1d dendrites (hereafter referred to as the DA1/VA1d dendritic pair), undergo rotational migration of ~45 ̊ around each other to attain their final adult positions [11]. To further unravel the mechanisms of PN dendritic targeting, we have screened for more mutations that disrupt the rotation of the DA1/VA1d dendritic pair
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