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

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) neur...

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Main Authors: Conrad M. Tenenbaum, Mala Misra, Rebecca A. Alizzi, Elizabeth R. Gavis
Format: Article
Language:English
Published: Elsevier 2017-09-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124717312627
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spelling doaj-f64951baa6d946ad928324f3870ca89a2020-11-24T21:47:22ZengElsevierCell Reports2211-12472017-09-0120133043305610.1016/j.celrep.2017.09.001Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory NeuronsConrad M. Tenenbaum0Mala Misra1Rebecca A. Alizzi2Elizabeth R. Gavis3Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USADepartment of Molecular Biology, Princeton University, Princeton, NJ 08544, USADepartment of Molecular Biology, Princeton University, Princeton, NJ 08544, USADepartment of Molecular Biology, Princeton University, Princeton, NJ 08544, USASpatial 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.http://www.sciencedirect.com/science/article/pii/S2211124717312627Drosophiladendrite morphogenesisdendritic arborization neuronneuronal developmentCoracleadhesion
collection DOAJ
language English
format Article
sources DOAJ
author Conrad M. Tenenbaum
Mala Misra
Rebecca A. Alizzi
Elizabeth R. Gavis
spellingShingle Conrad M. Tenenbaum
Mala Misra
Rebecca A. Alizzi
Elizabeth R. Gavis
Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons
Cell Reports
Drosophila
dendrite morphogenesis
dendritic arborization neuron
neuronal development
Coracle
adhesion
author_facet Conrad M. Tenenbaum
Mala Misra
Rebecca A. Alizzi
Elizabeth R. Gavis
author_sort Conrad M. Tenenbaum
title Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons
title_short Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons
title_full Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons
title_fullStr Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons
title_full_unstemmed Enclosure of Dendrites by Epidermal Cells Restricts Branching and Permits Coordinated Development of Spatially Overlapping Sensory Neurons
title_sort enclosure of dendrites by epidermal cells restricts branching and permits coordinated development of spatially overlapping sensory neurons
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2017-09-01
description 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.
topic Drosophila
dendrite morphogenesis
dendritic arborization neuron
neuronal development
Coracle
adhesion
url http://www.sciencedirect.com/science/article/pii/S2211124717312627
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AT rebeccaaalizzi enclosureofdendritesbyepidermalcellsrestrictsbranchingandpermitscoordinateddevelopmentofspatiallyoverlappingsensoryneurons
AT elizabethrgavis enclosureofdendritesbyepidermalcellsrestrictsbranchingandpermitscoordinateddevelopmentofspatiallyoverlappingsensoryneurons
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