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A multicellular rosette-mediated collective dendrite extension

Coordination of neurite morphogenesis with surrounding tissues is crucial to the establishment of neural circuits, but the underlying cellular and molecular mechanisms remain poorly understood. We show that neurons in a C. elegans sensory organ, called the amphid, undergo a collective dendrite exten...

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Detalles Bibliográficos
Autores principales: Fan, Li, Kovacevic, Ismar, Heiman, Maxwell G, Bao, Zhirong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6400498/
https://www.ncbi.nlm.nih.gov/pubmed/30767892
http://dx.doi.org/10.7554/eLife.38065
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author Fan, Li
Kovacevic, Ismar
Heiman, Maxwell G
Bao, Zhirong
author_facet Fan, Li
Kovacevic, Ismar
Heiman, Maxwell G
Bao, Zhirong
author_sort Fan, Li
collection PubMed
description Coordination of neurite morphogenesis with surrounding tissues is crucial to the establishment of neural circuits, but the underlying cellular and molecular mechanisms remain poorly understood. We show that neurons in a C. elegans sensory organ, called the amphid, undergo a collective dendrite extension to form the sensory nerve. The amphid neurons first assemble into a multicellular rosette. The vertex of the rosette, which becomes the dendrite tips, is attached to the anteriorly migrating epidermis and carried to the sensory depression, extruding the dendrites away from the neuronal cell bodies. Multiple adhesion molecules including DYF-7, SAX-7, HMR-1 and DLG-1 function redundantly in rosette-to-epidermis attachment. PAR-6 is localized to the rosette vertex and dendrite tips, and promotes DYF-7 localization and dendrite extension. Our results suggest a collective mechanism of neurite extension that is distinct from the classical pioneer-follower model and highlight the role of mechanical cues from surrounding tissues in shaping neurites.
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spelling pubmed-64004982019-03-06 A multicellular rosette-mediated collective dendrite extension Fan, Li Kovacevic, Ismar Heiman, Maxwell G Bao, Zhirong eLife Neuroscience Coordination of neurite morphogenesis with surrounding tissues is crucial to the establishment of neural circuits, but the underlying cellular and molecular mechanisms remain poorly understood. We show that neurons in a C. elegans sensory organ, called the amphid, undergo a collective dendrite extension to form the sensory nerve. The amphid neurons first assemble into a multicellular rosette. The vertex of the rosette, which becomes the dendrite tips, is attached to the anteriorly migrating epidermis and carried to the sensory depression, extruding the dendrites away from the neuronal cell bodies. Multiple adhesion molecules including DYF-7, SAX-7, HMR-1 and DLG-1 function redundantly in rosette-to-epidermis attachment. PAR-6 is localized to the rosette vertex and dendrite tips, and promotes DYF-7 localization and dendrite extension. Our results suggest a collective mechanism of neurite extension that is distinct from the classical pioneer-follower model and highlight the role of mechanical cues from surrounding tissues in shaping neurites. eLife Sciences Publications, Ltd 2019-02-15 /pmc/articles/PMC6400498/ /pubmed/30767892 http://dx.doi.org/10.7554/eLife.38065 Text en © 2019, Fan et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Fan, Li
Kovacevic, Ismar
Heiman, Maxwell G
Bao, Zhirong
A multicellular rosette-mediated collective dendrite extension
title A multicellular rosette-mediated collective dendrite extension
title_full A multicellular rosette-mediated collective dendrite extension
title_fullStr A multicellular rosette-mediated collective dendrite extension
title_full_unstemmed A multicellular rosette-mediated collective dendrite extension
title_short A multicellular rosette-mediated collective dendrite extension
title_sort multicellular rosette-mediated collective dendrite extension
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6400498/
https://www.ncbi.nlm.nih.gov/pubmed/30767892
http://dx.doi.org/10.7554/eLife.38065
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