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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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 |
work_keys_str_mv |
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