An Integrated Cytoskeletal Model of Neurite Outgrowth

Neurite outgrowth underlies the wiring of the nervous system during development and regeneration. Despite a significant body of research, the underlying cytoskeletal mechanics of growth and guidance are not fully understood, and the relative contributions of individual cytoskeletal processes to neur...

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Main Authors: Kyle E. Miller, Daniel M. Suter
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-11-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncel.2018.00447/full
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author Kyle E. Miller
Daniel M. Suter
Daniel M. Suter
Daniel M. Suter
Daniel M. Suter
author_facet Kyle E. Miller
Daniel M. Suter
Daniel M. Suter
Daniel M. Suter
Daniel M. Suter
author_sort Kyle E. Miller
collection DOAJ
description Neurite outgrowth underlies the wiring of the nervous system during development and regeneration. Despite a significant body of research, the underlying cytoskeletal mechanics of growth and guidance are not fully understood, and the relative contributions of individual cytoskeletal processes to neurite growth are controversial. Here, we review the structural organization and biophysical properties of neurons to make a semi-quantitative comparison of the relative contributions of different processes to neurite growth. From this, we develop the idea that neurons are active fluids, which generate strong contractile forces in the growth cone and weaker contractile forces along the axon. As a result of subcellular gradients in forces and material properties, actin flows rapidly rearward in the growth cone periphery, and microtubules flow forward in bulk along the axon. With this framework, an integrated model of neurite outgrowth is proposed that hopefully will guide new approaches to stimulate neuronal growth.
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spelling doaj.art-d38c1ce1fa0a48f2aa6b7671043074382022-12-22T03:15:59ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022018-11-011210.3389/fncel.2018.00447424803An Integrated Cytoskeletal Model of Neurite OutgrowthKyle E. Miller0Daniel M. Suter1Daniel M. Suter2Daniel M. Suter3Daniel M. Suter4Department of Integrative Biology, Michigan State University, East Lansing, MI, United StatesDepartment of Biological Sciences, Purdue University, West Lafayette, IN, United StatesPurdue Institute for Integrative Neuroscience, Purdue University, West Lafayette, IN, United StatesBindley Bioscience Center, Purdue University, West Lafayette, IN, United StatesBirck Nanotechnology Center, Purdue University, West Lafayette, IN, United StatesNeurite outgrowth underlies the wiring of the nervous system during development and regeneration. Despite a significant body of research, the underlying cytoskeletal mechanics of growth and guidance are not fully understood, and the relative contributions of individual cytoskeletal processes to neurite growth are controversial. Here, we review the structural organization and biophysical properties of neurons to make a semi-quantitative comparison of the relative contributions of different processes to neurite growth. From this, we develop the idea that neurons are active fluids, which generate strong contractile forces in the growth cone and weaker contractile forces along the axon. As a result of subcellular gradients in forces and material properties, actin flows rapidly rearward in the growth cone periphery, and microtubules flow forward in bulk along the axon. With this framework, an integrated model of neurite outgrowth is proposed that hopefully will guide new approaches to stimulate neuronal growth.https://www.frontiersin.org/article/10.3389/fncel.2018.00447/fullactive matteractinaxonal elongationaxonal transportdyneingrowth cone
spellingShingle Kyle E. Miller
Daniel M. Suter
Daniel M. Suter
Daniel M. Suter
Daniel M. Suter
An Integrated Cytoskeletal Model of Neurite Outgrowth
Frontiers in Cellular Neuroscience
active matter
actin
axonal elongation
axonal transport
dynein
growth cone
title An Integrated Cytoskeletal Model of Neurite Outgrowth
title_full An Integrated Cytoskeletal Model of Neurite Outgrowth
title_fullStr An Integrated Cytoskeletal Model of Neurite Outgrowth
title_full_unstemmed An Integrated Cytoskeletal Model of Neurite Outgrowth
title_short An Integrated Cytoskeletal Model of Neurite Outgrowth
title_sort integrated cytoskeletal model of neurite outgrowth
topic active matter
actin
axonal elongation
axonal transport
dynein
growth cone
url https://www.frontiersin.org/article/10.3389/fncel.2018.00447/full
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