Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons

• Published in: Cell reports (Cambridge) Vol. 20; no. 13; pp. 3043 - 3056
• Main Authors: Tenenbaum, Conrad M., Misra, Mala, Alizzi, Rebecca A., Gavis, Elizabeth R.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 26-09-2017; Elsevier
• Subjects: adhesion; Animals; Coracle; dendrite morphogenesis; Dendrites - metabolism; dendritic arborization neuron; Drosophila; Epidermis - metabolism; Membrane Proteins - metabolism; neuronal development; Sensory Receptor Cells - metabolism; neuronal development; dendritic arborization neuron; adhesion; dendrite morphogenesis; Drosophila; Coracle
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2017.09.001

Spatial arrangement of different neuron types within a territory is essential to neuronal development and function. How development of different neuron types is coordinated for spatial coexistence is poorly understood. In Drosophila, dendrites of four classes of dendritic arborization (C1–C4da) neurons innervate overlapping receptive fields within the larval epidermis. These dendrites are intermittently enclosed by epidermal cells, with different classes exhibiting varying degrees of enclosure. The role of enclosure in neuronal development and its underlying mechanism remain unknown. We show that the membrane-associated protein Coracle acts in C4da neurons and epidermal cells to locally restrict dendrite branching and outgrowth by promoting enclosure. Loss of C4da neuron enclosure results in excessive branching and growth of C4da neuron dendrites and retraction of C1da neuron dendrites due to local inhibitory interactions between neurons. We propose that enclosure of dendrites by epidermal cells is a developmental mechanism for coordinated innervation of shared receptive fields.
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•Coracle is required for enclosure of C4da neuron dendrites by epidermal cells•C4da neuron dendrites exhibit local epithelial-like characteristics•Coracle-mediated enclosure locally restricts dendrite branching•Enclosure maximizes field coverage among different classes of da neurons
Tenenbaum et al. show that the membrane-associated protein Coracle locally restricts sensory neuron dendrite branching by promoting enclosure of dendrite segments by epidermal cells. Enclosure counteracts inhibitory interactions between different classes of sensory neurons, suggesting it provides a developmental mechanism for coordinated innervation of shared receptive fields.