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Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway

Sensory neurons with common functions are often nonrandomly arranged and form dendritic territories in stereotypic spatial patterns throughout the nervous system, yet molecular mechanisms of how neurons specify dendritic territories remain largely unknown. In Drosophila larvae, dendrites of class IV...

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Autores principales: Yasunaga, Kei-ichiro, Tezuka, Akane, Ishikawa, Natsuko, Dairyo, Yusuke, Togashi, Kazuya, Koizumi, Hiroyuki, Emoto, Kazuo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4561484/
https://www.ncbi.nlm.nih.gov/pubmed/26302791
http://dx.doi.org/10.1101/gad.262592.115
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author Yasunaga, Kei-ichiro
Tezuka, Akane
Ishikawa, Natsuko
Dairyo, Yusuke
Togashi, Kazuya
Koizumi, Hiroyuki
Emoto, Kazuo
author_facet Yasunaga, Kei-ichiro
Tezuka, Akane
Ishikawa, Natsuko
Dairyo, Yusuke
Togashi, Kazuya
Koizumi, Hiroyuki
Emoto, Kazuo
author_sort Yasunaga, Kei-ichiro
collection PubMed
description Sensory neurons with common functions are often nonrandomly arranged and form dendritic territories in stereotypic spatial patterns throughout the nervous system, yet molecular mechanisms of how neurons specify dendritic territories remain largely unknown. In Drosophila larvae, dendrites of class IV sensory (C4da) neurons completely but nonredundantly cover the whole epidermis, and the boundaries of these tiled dendritic fields are specified through repulsive interactions between homotypic dendrites. Here we report that, unlike the larval C4da neurons, adult C4da neurons rely on both dendritic repulsive interactions and external positional cues to delimit the boundaries of their dendritic fields. We identify Wnt5 derived from sternites, the ventral-most part of the adult abdominal epidermis, as the critical determinant for the ventral boundaries. Further genetic data indicate that Wnt5 promotes dendrite termination on the periphery of sternites through the Ryk receptor family kinase Derailed (Drl) and the Rho GTPase guanine nucleotide exchange factor Trio in C4da neurons. Our findings thus uncover the dendritic contact-independent mechanism that is required for dendritic boundary specification and suggest that combinatory actions of the dendritic contact-dependent and -independent mechanisms may ensure appropriate dendritic territories of a given neuron.
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spelling pubmed-45614842016-02-15 Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway Yasunaga, Kei-ichiro Tezuka, Akane Ishikawa, Natsuko Dairyo, Yusuke Togashi, Kazuya Koizumi, Hiroyuki Emoto, Kazuo Genes Dev Research Paper Sensory neurons with common functions are often nonrandomly arranged and form dendritic territories in stereotypic spatial patterns throughout the nervous system, yet molecular mechanisms of how neurons specify dendritic territories remain largely unknown. In Drosophila larvae, dendrites of class IV sensory (C4da) neurons completely but nonredundantly cover the whole epidermis, and the boundaries of these tiled dendritic fields are specified through repulsive interactions between homotypic dendrites. Here we report that, unlike the larval C4da neurons, adult C4da neurons rely on both dendritic repulsive interactions and external positional cues to delimit the boundaries of their dendritic fields. We identify Wnt5 derived from sternites, the ventral-most part of the adult abdominal epidermis, as the critical determinant for the ventral boundaries. Further genetic data indicate that Wnt5 promotes dendrite termination on the periphery of sternites through the Ryk receptor family kinase Derailed (Drl) and the Rho GTPase guanine nucleotide exchange factor Trio in C4da neurons. Our findings thus uncover the dendritic contact-independent mechanism that is required for dendritic boundary specification and suggest that combinatory actions of the dendritic contact-dependent and -independent mechanisms may ensure appropriate dendritic territories of a given neuron. Cold Spring Harbor Laboratory Press 2015-08-15 /pmc/articles/PMC4561484/ /pubmed/26302791 http://dx.doi.org/10.1101/gad.262592.115 Text en © 2015 Yasunaga et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research Paper
Yasunaga, Kei-ichiro
Tezuka, Akane
Ishikawa, Natsuko
Dairyo, Yusuke
Togashi, Kazuya
Koizumi, Hiroyuki
Emoto, Kazuo
Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway
title Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway
title_full Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway
title_fullStr Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway
title_full_unstemmed Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway
title_short Adult Drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the Wnt5–Drl signaling pathway
title_sort adult drosophila sensory neurons specify dendritic territories independently of dendritic contacts through the wnt5–drl signaling pathway
topic Research Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4561484/
https://www.ncbi.nlm.nih.gov/pubmed/26302791
http://dx.doi.org/10.1101/gad.262592.115
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