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

Conrad M. Tenenbaum, Mala Misra, Rebecca A. Alizzi, Elizabeth R. Gavis

Research output: Contribution to journalArticle

11 Scopus citations

Abstract

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. 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.

Original languageEnglish (US)
Pages (from-to)3043-3056
Number of pages14
JournalCell Reports
Volume20
Issue number13
DOIs
StatePublished - Sep 26 2017

All Science Journal Classification (ASJC) codes

  • Biochemistry, Genetics and Molecular Biology(all)

Keywords

  • Coracle
  • Drosophila
  • adhesion
  • dendrite morphogenesis
  • dendritic arborization neuron
  • neuronal development

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