Cargando…

Microtubules and motor proteins support zebrafish neuronal migration by directing cargo

Neuronal migration during development is necessary to form an ordered and functional brain. Postmitotic neurons require microtubules and dynein to move, but the mechanisms by which they contribute to migration are not fully characterized. Using tegmental hindbrain nuclei neurons in zebrafish embryos...

Descripción completa

Detalles Bibliográficos
Autores principales: Theisen, Ulrike, Ernst, Alexander U., Heyne, Ronja L.S., Ring, Tobias P., Thorn-Seshold, Oliver, Köster, Reinhard W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7659711/
https://www.ncbi.nlm.nih.gov/pubmed/32668451
http://dx.doi.org/10.1083/jcb.201908040
_version_ 1783608867646603264
author Theisen, Ulrike
Ernst, Alexander U.
Heyne, Ronja L.S.
Ring, Tobias P.
Thorn-Seshold, Oliver
Köster, Reinhard W.
author_facet Theisen, Ulrike
Ernst, Alexander U.
Heyne, Ronja L.S.
Ring, Tobias P.
Thorn-Seshold, Oliver
Köster, Reinhard W.
author_sort Theisen, Ulrike
collection PubMed
description Neuronal migration during development is necessary to form an ordered and functional brain. Postmitotic neurons require microtubules and dynein to move, but the mechanisms by which they contribute to migration are not fully characterized. Using tegmental hindbrain nuclei neurons in zebrafish embryos together with subcellular imaging, optogenetics, and photopharmacology, we show that, in vivo, the centrosome’s position relative to the nucleus is not linked to greatest motility in this cell type. Nevertheless, microtubules, dynein, and kinesin-1 are essential for migration, and we find that interference with endosome formation or the Golgi apparatus impairs migration to a similar extent as disrupting microtubules. In addition, an imbalance in the traffic of the model cargo Cadherin-2 also reduces neuronal migration. These results lead us to propose that microtubules act as cargo carriers to control spatiotemporal protein distribution, which in turn controls motility. This adds crucial insights into the variety of ways that microtubules can support successful neuronal migration in vivo.
format Online
Article
Text
id pubmed-7659711
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-76597112021-04-05 Microtubules and motor proteins support zebrafish neuronal migration by directing cargo Theisen, Ulrike Ernst, Alexander U. Heyne, Ronja L.S. Ring, Tobias P. Thorn-Seshold, Oliver Köster, Reinhard W. J Cell Biol Article Neuronal migration during development is necessary to form an ordered and functional brain. Postmitotic neurons require microtubules and dynein to move, but the mechanisms by which they contribute to migration are not fully characterized. Using tegmental hindbrain nuclei neurons in zebrafish embryos together with subcellular imaging, optogenetics, and photopharmacology, we show that, in vivo, the centrosome’s position relative to the nucleus is not linked to greatest motility in this cell type. Nevertheless, microtubules, dynein, and kinesin-1 are essential for migration, and we find that interference with endosome formation or the Golgi apparatus impairs migration to a similar extent as disrupting microtubules. In addition, an imbalance in the traffic of the model cargo Cadherin-2 also reduces neuronal migration. These results lead us to propose that microtubules act as cargo carriers to control spatiotemporal protein distribution, which in turn controls motility. This adds crucial insights into the variety of ways that microtubules can support successful neuronal migration in vivo. Rockefeller University Press 2020-07-15 /pmc/articles/PMC7659711/ /pubmed/32668451 http://dx.doi.org/10.1083/jcb.201908040 Text en © 2020 Theisen et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Theisen, Ulrike
Ernst, Alexander U.
Heyne, Ronja L.S.
Ring, Tobias P.
Thorn-Seshold, Oliver
Köster, Reinhard W.
Microtubules and motor proteins support zebrafish neuronal migration by directing cargo
title Microtubules and motor proteins support zebrafish neuronal migration by directing cargo
title_full Microtubules and motor proteins support zebrafish neuronal migration by directing cargo
title_fullStr Microtubules and motor proteins support zebrafish neuronal migration by directing cargo
title_full_unstemmed Microtubules and motor proteins support zebrafish neuronal migration by directing cargo
title_short Microtubules and motor proteins support zebrafish neuronal migration by directing cargo
title_sort microtubules and motor proteins support zebrafish neuronal migration by directing cargo
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7659711/
https://www.ncbi.nlm.nih.gov/pubmed/32668451
http://dx.doi.org/10.1083/jcb.201908040
work_keys_str_mv AT theisenulrike microtubulesandmotorproteinssupportzebrafishneuronalmigrationbydirectingcargo
AT ernstalexanderu microtubulesandmotorproteinssupportzebrafishneuronalmigrationbydirectingcargo
AT heyneronjals microtubulesandmotorproteinssupportzebrafishneuronalmigrationbydirectingcargo
AT ringtobiasp microtubulesandmotorproteinssupportzebrafishneuronalmigrationbydirectingcargo
AT thornsesholdoliver microtubulesandmotorproteinssupportzebrafishneuronalmigrationbydirectingcargo
AT kosterreinhardw microtubulesandmotorproteinssupportzebrafishneuronalmigrationbydirectingcargo