Neurite elongation is highly correlated with bulk forward translocation of microtubules

Abstract During the development of the nervous system and regeneration following injury, microtubules (MTs) are required for neurite elongation. Whether this elongation occurs primarily through tubulin assembly at the tip of the axon, the transport of individual MTs, or because MTs translocate forwa...

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Autores principales: Ahmad I. M. Athamneh, Yingpei He, Phillip Lamoureux, Lucas Fix, Daniel M. Suter, Kyle E. Miller
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Lenguaje:EN
Publicado: Nature Portfolio 2017
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Acceso en línea:https://doaj.org/article/4663e944c62c40b2b7c3b70ccabaadc5
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spelling oai:doaj.org-article:4663e944c62c40b2b7c3b70ccabaadc52021-12-02T12:30:35ZNeurite elongation is highly correlated with bulk forward translocation of microtubules10.1038/s41598-017-07402-62045-2322https://doaj.org/article/4663e944c62c40b2b7c3b70ccabaadc52017-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-07402-6https://doaj.org/toc/2045-2322Abstract During the development of the nervous system and regeneration following injury, microtubules (MTs) are required for neurite elongation. Whether this elongation occurs primarily through tubulin assembly at the tip of the axon, the transport of individual MTs, or because MTs translocate forward in bulk is unclear. Using fluorescent speckle microscopy (FSM), differential interference contrast (DIC), and phase contrast microscopy, we tracked the movement of MTs, phase dense material, and docked mitochondria in chick sensory and Aplysia bag cell neurons growing rapidly on physiological substrates. In all cases, we find that MTs and other neuritic components move forward in bulk at a rate that on average matches the velocity of neurite elongation. To better understand whether and why MT assembly is required for bulk translocation, we disrupted it with nocodazole. We found this blocked the forward bulk advance of material along the neurite and was paired with a transient increase in axonal tension. This indicates that disruption of MT dynamics interferes with neurite outgrowth, not by disrupting the net assembly of MTs at the growth cone, but rather because it alters the balance of forces that power the bulk forward translocation of MTs.Ahmad I. M. AthamnehYingpei HePhillip LamoureuxLucas FixDaniel M. SuterKyle E. MillerNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-13 (2017)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Ahmad I. M. Athamneh
Yingpei He
Phillip Lamoureux
Lucas Fix
Daniel M. Suter
Kyle E. Miller
Neurite elongation is highly correlated with bulk forward translocation of microtubules
description Abstract During the development of the nervous system and regeneration following injury, microtubules (MTs) are required for neurite elongation. Whether this elongation occurs primarily through tubulin assembly at the tip of the axon, the transport of individual MTs, or because MTs translocate forward in bulk is unclear. Using fluorescent speckle microscopy (FSM), differential interference contrast (DIC), and phase contrast microscopy, we tracked the movement of MTs, phase dense material, and docked mitochondria in chick sensory and Aplysia bag cell neurons growing rapidly on physiological substrates. In all cases, we find that MTs and other neuritic components move forward in bulk at a rate that on average matches the velocity of neurite elongation. To better understand whether and why MT assembly is required for bulk translocation, we disrupted it with nocodazole. We found this blocked the forward bulk advance of material along the neurite and was paired with a transient increase in axonal tension. This indicates that disruption of MT dynamics interferes with neurite outgrowth, not by disrupting the net assembly of MTs at the growth cone, but rather because it alters the balance of forces that power the bulk forward translocation of MTs.
format article
author Ahmad I. M. Athamneh
Yingpei He
Phillip Lamoureux
Lucas Fix
Daniel M. Suter
Kyle E. Miller
author_facet Ahmad I. M. Athamneh
Yingpei He
Phillip Lamoureux
Lucas Fix
Daniel M. Suter
Kyle E. Miller
author_sort Ahmad I. M. Athamneh
title Neurite elongation is highly correlated with bulk forward translocation of microtubules
title_short Neurite elongation is highly correlated with bulk forward translocation of microtubules
title_full Neurite elongation is highly correlated with bulk forward translocation of microtubules
title_fullStr Neurite elongation is highly correlated with bulk forward translocation of microtubules
title_full_unstemmed Neurite elongation is highly correlated with bulk forward translocation of microtubules
title_sort neurite elongation is highly correlated with bulk forward translocation of microtubules
publisher Nature Portfolio
publishDate 2017
url https://doaj.org/article/4663e944c62c40b2b7c3b70ccabaadc5
work_keys_str_mv AT ahmadimathamneh neuriteelongationishighlycorrelatedwithbulkforwardtranslocationofmicrotubules
AT yingpeihe neuriteelongationishighlycorrelatedwithbulkforwardtranslocationofmicrotubules
AT philliplamoureux neuriteelongationishighlycorrelatedwithbulkforwardtranslocationofmicrotubules
AT lucasfix neuriteelongationishighlycorrelatedwithbulkforwardtranslocationofmicrotubules
AT danielmsuter neuriteelongationishighlycorrelatedwithbulkforwardtranslocationofmicrotubules
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