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Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons

Growth cones of elongating neurites exert force against the external environment, but little is known about the role of force in outgrowth or its relationship to the mechanical organization of neurons. We used traction force microscopy to examine patterns of force in growth cones of regenerating Apl...

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Autores principales: Hyland, Callen, Mertz, Aaron F., Forscher, Paul, Dufresne, Eric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4019958/
https://www.ncbi.nlm.nih.gov/pubmed/24825441
http://dx.doi.org/10.1038/srep04961
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author Hyland, Callen
Mertz, Aaron F.
Forscher, Paul
Dufresne, Eric
author_facet Hyland, Callen
Mertz, Aaron F.
Forscher, Paul
Dufresne, Eric
author_sort Hyland, Callen
collection PubMed
description Growth cones of elongating neurites exert force against the external environment, but little is known about the role of force in outgrowth or its relationship to the mechanical organization of neurons. We used traction force microscopy to examine patterns of force in growth cones of regenerating Aplysia bag cell neurons. We find that traction is highest in the peripheral actin-rich domain and internal stress reaches a plateau near the transition between peripheral and central microtubule-rich domains. Integrating stress over the area of the growth cone reveals that total scalar force increases with area but net tension on the neurite does not. Tensions fall within a limited range while a substantial fraction of the total force can be balanced locally within the growth cone. Although traction continuously redistributes during extension and retraction of the peripheral domain, tension is stable over time, suggesting that tension is a tightly regulated property of the neurite independent of growth cone dynamics. We observe that redistribution of traction in the peripheral domain can reorient the end of the neurite shaft. This suggests a role for off-axis force in growth cone turning and neuronal guidance.
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spelling pubmed-40199582014-05-14 Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons Hyland, Callen Mertz, Aaron F. Forscher, Paul Dufresne, Eric Sci Rep Article Growth cones of elongating neurites exert force against the external environment, but little is known about the role of force in outgrowth or its relationship to the mechanical organization of neurons. We used traction force microscopy to examine patterns of force in growth cones of regenerating Aplysia bag cell neurons. We find that traction is highest in the peripheral actin-rich domain and internal stress reaches a plateau near the transition between peripheral and central microtubule-rich domains. Integrating stress over the area of the growth cone reveals that total scalar force increases with area but net tension on the neurite does not. Tensions fall within a limited range while a substantial fraction of the total force can be balanced locally within the growth cone. Although traction continuously redistributes during extension and retraction of the peripheral domain, tension is stable over time, suggesting that tension is a tightly regulated property of the neurite independent of growth cone dynamics. We observe that redistribution of traction in the peripheral domain can reorient the end of the neurite shaft. This suggests a role for off-axis force in growth cone turning and neuronal guidance. Nature Publishing Group 2014-05-14 /pmc/articles/PMC4019958/ /pubmed/24825441 http://dx.doi.org/10.1038/srep04961 Text en Copyright © 2014, Macmillan Publishers Limited. All rights reserved http://creativecommons.org/licenses/by-nc-nd/3.0/ This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. The images in this article are included in the article's Creative Commons license, unless indicated otherwise in the image credit; if the image is not included under the Creative Commons license, users will need to obtain permission from the license holder in order to reproduce the image. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/
spellingShingle Article
Hyland, Callen
Mertz, Aaron F.
Forscher, Paul
Dufresne, Eric
Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons
title Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons
title_full Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons
title_fullStr Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons
title_full_unstemmed Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons
title_short Dynamic peripheral traction forces balance stable neurite tension in regenerating Aplysia bag cell neurons
title_sort dynamic peripheral traction forces balance stable neurite tension in regenerating aplysia bag cell neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4019958/
https://www.ncbi.nlm.nih.gov/pubmed/24825441
http://dx.doi.org/10.1038/srep04961
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