Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons
In this study, we investigated how microtubule motors organize microtubules in Drosophila neurons. We showed that, during the initial stages of axon outgrowth, microtubules display mixed polarity and minus-end-out microtubules push the tip of the axon, consistent with kinesin-1 driving outgrowth by...
Main Authors: | , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2015-11-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/10140 |
id |
doaj-2f1c7c4131f6428abafa3950b78e11a8 |
---|---|
record_format |
Article |
spelling |
doaj-2f1c7c4131f6428abafa3950b78e11a82021-05-05T00:11:26ZengeLife Sciences Publications LtdeLife2050-084X2015-11-01410.7554/eLife.10140Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neuronsUrko del Castillo0Michael Winding1Wen Lu2Vladimir I Gelfand3Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesDepartment of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesDepartment of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesDepartment of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesIn this study, we investigated how microtubule motors organize microtubules in Drosophila neurons. We showed that, during the initial stages of axon outgrowth, microtubules display mixed polarity and minus-end-out microtubules push the tip of the axon, consistent with kinesin-1 driving outgrowth by sliding antiparallel microtubules. At later stages, the microtubule orientation in the axon switches from mixed to uniform polarity with plus-end-out. Dynein knockdown prevents this rearrangement and results in microtubules of mixed orientation in axons and accumulation of microtubule minus-ends at axon tips. Microtubule reorganization requires recruitment of dynein to the actin cortex, as actin depolymerization phenocopies dynein depletion, and direct recruitment of dynein to the membrane bypasses the actin requirement. Our results show that cortical dynein slides ‘minus-end-out’ microtubules from the axon, generating uniform microtubule arrays. We speculate that differences in microtubule orientation between axons and dendrites could be dictated by differential activity of cortical dynein.https://elifesciences.org/articles/10140microtubulesneuronaxonskinesindyneinactin |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Urko del Castillo Michael Winding Wen Lu Vladimir I Gelfand |
spellingShingle |
Urko del Castillo Michael Winding Wen Lu Vladimir I Gelfand Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons eLife microtubules neuron axons kinesin dynein actin |
author_facet |
Urko del Castillo Michael Winding Wen Lu Vladimir I Gelfand |
author_sort |
Urko del Castillo |
title |
Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons |
title_short |
Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons |
title_full |
Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons |
title_fullStr |
Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons |
title_full_unstemmed |
Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons |
title_sort |
interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in drosophila neurons |
publisher |
eLife Sciences Publications Ltd |
series |
eLife |
issn |
2050-084X |
publishDate |
2015-11-01 |
description |
In this study, we investigated how microtubule motors organize microtubules in Drosophila neurons. We showed that, during the initial stages of axon outgrowth, microtubules display mixed polarity and minus-end-out microtubules push the tip of the axon, consistent with kinesin-1 driving outgrowth by sliding antiparallel microtubules. At later stages, the microtubule orientation in the axon switches from mixed to uniform polarity with plus-end-out. Dynein knockdown prevents this rearrangement and results in microtubules of mixed orientation in axons and accumulation of microtubule minus-ends at axon tips. Microtubule reorganization requires recruitment of dynein to the actin cortex, as actin depolymerization phenocopies dynein depletion, and direct recruitment of dynein to the membrane bypasses the actin requirement. Our results show that cortical dynein slides ‘minus-end-out’ microtubules from the axon, generating uniform microtubule arrays. We speculate that differences in microtubule orientation between axons and dendrites could be dictated by differential activity of cortical dynein. |
topic |
microtubules neuron axons kinesin dynein actin |
url |
https://elifesciences.org/articles/10140 |
work_keys_str_mv |
AT urkodelcastillo interplaybetweenkinesin1andcorticaldyneinduringaxonaloutgrowthandmicrotubuleorganizationindrosophilaneurons AT michaelwinding interplaybetweenkinesin1andcorticaldyneinduringaxonaloutgrowthandmicrotubuleorganizationindrosophilaneurons AT wenlu interplaybetweenkinesin1andcorticaldyneinduringaxonaloutgrowthandmicrotubuleorganizationindrosophilaneurons AT vladimirigelfand interplaybetweenkinesin1andcorticaldyneinduringaxonaloutgrowthandmicrotubuleorganizationindrosophilaneurons |
_version_ |
1721476478067015680 |