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Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A

The kinesin-3 motor KIF1A is in charge of vesicular transport in neuronal axons. Its single-headed form is known to be very inefficient due to the presence of a diffusive state in the mechanochemical cycle. However, recent theoretical studies have suggested that these motors could largely enhance fo...

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Detalles Bibliográficos
Autores principales: Oriola, David, Roth, Sophie, Dogterom, Marileen, Casademunt, Jaume
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Pub. Group 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4557341/
https://www.ncbi.nlm.nih.gov/pubmed/26268542
http://dx.doi.org/10.1038/ncomms9025
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author Oriola, David
Roth, Sophie
Dogterom, Marileen
Casademunt, Jaume
author_facet Oriola, David
Roth, Sophie
Dogterom, Marileen
Casademunt, Jaume
author_sort Oriola, David
collection PubMed
description The kinesin-3 motor KIF1A is in charge of vesicular transport in neuronal axons. Its single-headed form is known to be very inefficient due to the presence of a diffusive state in the mechanochemical cycle. However, recent theoretical studies have suggested that these motors could largely enhance force generation by working in teams. Here we test this prediction by challenging single-headed KIF1A to extract membrane tubes from giant vesicles along microtubule filaments in a minimal in vitro system. Remarkably, not only KIF1A motors are able to extract tubes but they feature a novel phenomenon: tubes are wound around microtubules forming tubular helices. This finding reveals an unforeseen combination of cooperative force generation and self-organized manoeuvreing capability, suggesting that the diffusive state may be a key ingredient for collective motor performance under demanding traffic conditions. Hence, we conclude that KIF1A is a genuinely cooperative motor, possibly explaining its specificity to axonal trafficking.
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spelling pubmed-45573412015-09-14 Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A Oriola, David Roth, Sophie Dogterom, Marileen Casademunt, Jaume Nat Commun Article The kinesin-3 motor KIF1A is in charge of vesicular transport in neuronal axons. Its single-headed form is known to be very inefficient due to the presence of a diffusive state in the mechanochemical cycle. However, recent theoretical studies have suggested that these motors could largely enhance force generation by working in teams. Here we test this prediction by challenging single-headed KIF1A to extract membrane tubes from giant vesicles along microtubule filaments in a minimal in vitro system. Remarkably, not only KIF1A motors are able to extract tubes but they feature a novel phenomenon: tubes are wound around microtubules forming tubular helices. This finding reveals an unforeseen combination of cooperative force generation and self-organized manoeuvreing capability, suggesting that the diffusive state may be a key ingredient for collective motor performance under demanding traffic conditions. Hence, we conclude that KIF1A is a genuinely cooperative motor, possibly explaining its specificity to axonal trafficking. Nature Pub. Group 2015-08-13 /pmc/articles/PMC4557341/ /pubmed/26268542 http://dx.doi.org/10.1038/ncomms9025 Text en Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Oriola, David
Roth, Sophie
Dogterom, Marileen
Casademunt, Jaume
Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A
title Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A
title_full Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A
title_fullStr Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A
title_full_unstemmed Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A
title_short Formation of helical membrane tubes around microtubules by single-headed kinesin KIF1A
title_sort formation of helical membrane tubes around microtubules by single-headed kinesin kif1a
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4557341/
https://www.ncbi.nlm.nih.gov/pubmed/26268542
http://dx.doi.org/10.1038/ncomms9025
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