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Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69

To remodel functional neuronal connectivity, neurons often alter dendrite arbors through elimination and subsequent regeneration of dendritic branches. However, the intrinsic mechanisms underlying this developmentally programmed dendrite regeneration and whether it shares common machinery with injur...

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Autores principales: Kitatani, Yasuko, Tezuka, Akane, Hasegawa, Eri, Yanagi, Satoyoshi, Togashi, Kazuya, Tsuji, Masato, Kondo, Shu, Parrish, Jay Z., Emoto, Kazuo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439810/
https://www.ncbi.nlm.nih.gov/pubmed/32764744
http://dx.doi.org/10.1371/journal.pgen.1008942
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author Kitatani, Yasuko
Tezuka, Akane
Hasegawa, Eri
Yanagi, Satoyoshi
Togashi, Kazuya
Tsuji, Masato
Kondo, Shu
Parrish, Jay Z.
Emoto, Kazuo
author_facet Kitatani, Yasuko
Tezuka, Akane
Hasegawa, Eri
Yanagi, Satoyoshi
Togashi, Kazuya
Tsuji, Masato
Kondo, Shu
Parrish, Jay Z.
Emoto, Kazuo
author_sort Kitatani, Yasuko
collection PubMed
description To remodel functional neuronal connectivity, neurons often alter dendrite arbors through elimination and subsequent regeneration of dendritic branches. However, the intrinsic mechanisms underlying this developmentally programmed dendrite regeneration and whether it shares common machinery with injury-induced regeneration remain largely unknown. Drosophila class IV dendrite arborization (C4da) sensory neurons regenerate adult-specific dendrites after eliminating larval dendrites during metamorphosis. Here we show that the microRNA miR-87 is a critical regulator of dendrite regeneration in Drosophila. miR-87 knockout impairs dendrite regeneration after developmentally-programmed pruning, whereas miR-87 overexpression in C4da neurons leads to precocious initiation of dendrite regeneration. Genetic analyses indicate that the transcriptional repressor Tramtrack69 (Ttk69) is a functional target for miR-87-mediated repression as ttk69 expression is increased in miR-87 knockout neurons and reducing ttk69 expression restores dendrite regeneration to mutants lacking miR-87 function. We further show that miR-87 is required for dendrite regeneration after acute injury in the larval stage, providing a mechanistic link between developmentally programmed and injury-induced dendrite regeneration. These findings thus indicate that miR-87 promotes dendrite regrowth during regeneration at least in part through suppressing Ttk69 in Drosophila sensory neurons and suggest that developmental and injury-induced dendrite regeneration share a common intrinsic mechanism to reactivate dendrite growth.
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spelling pubmed-74398102020-08-26 Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69 Kitatani, Yasuko Tezuka, Akane Hasegawa, Eri Yanagi, Satoyoshi Togashi, Kazuya Tsuji, Masato Kondo, Shu Parrish, Jay Z. Emoto, Kazuo PLoS Genet Research Article To remodel functional neuronal connectivity, neurons often alter dendrite arbors through elimination and subsequent regeneration of dendritic branches. However, the intrinsic mechanisms underlying this developmentally programmed dendrite regeneration and whether it shares common machinery with injury-induced regeneration remain largely unknown. Drosophila class IV dendrite arborization (C4da) sensory neurons regenerate adult-specific dendrites after eliminating larval dendrites during metamorphosis. Here we show that the microRNA miR-87 is a critical regulator of dendrite regeneration in Drosophila. miR-87 knockout impairs dendrite regeneration after developmentally-programmed pruning, whereas miR-87 overexpression in C4da neurons leads to precocious initiation of dendrite regeneration. Genetic analyses indicate that the transcriptional repressor Tramtrack69 (Ttk69) is a functional target for miR-87-mediated repression as ttk69 expression is increased in miR-87 knockout neurons and reducing ttk69 expression restores dendrite regeneration to mutants lacking miR-87 function. We further show that miR-87 is required for dendrite regeneration after acute injury in the larval stage, providing a mechanistic link between developmentally programmed and injury-induced dendrite regeneration. These findings thus indicate that miR-87 promotes dendrite regrowth during regeneration at least in part through suppressing Ttk69 in Drosophila sensory neurons and suggest that developmental and injury-induced dendrite regeneration share a common intrinsic mechanism to reactivate dendrite growth. Public Library of Science 2020-08-07 /pmc/articles/PMC7439810/ /pubmed/32764744 http://dx.doi.org/10.1371/journal.pgen.1008942 Text en © 2020 Kitatani et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Kitatani, Yasuko
Tezuka, Akane
Hasegawa, Eri
Yanagi, Satoyoshi
Togashi, Kazuya
Tsuji, Masato
Kondo, Shu
Parrish, Jay Z.
Emoto, Kazuo
Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
title Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
title_full Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
title_fullStr Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
title_full_unstemmed Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
title_short Drosophila miR-87 promotes dendrite regeneration by targeting the transcriptional repressor Tramtrack69
title_sort drosophila mir-87 promotes dendrite regeneration by targeting the transcriptional repressor tramtrack69
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7439810/
https://www.ncbi.nlm.nih.gov/pubmed/32764744
http://dx.doi.org/10.1371/journal.pgen.1008942
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