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Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability
Most mammalian neurons have a narrow axon, which constrains the passage of large cargoes such as autophagosomes that can be larger than the axon diameter. Radial axonal expansion must therefore occur to ensure efficient axonal trafficking. In this study, we reveal that the speed of various large car...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Rockefeller University Press
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7199852/ https://www.ncbi.nlm.nih.gov/pubmed/32182623 http://dx.doi.org/10.1083/jcb.201902001 |
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author | Wang, Tong Li, Wei Martin, Sally Papadopulos, Andreas Joensuu, Merja Liu, Chunxia Jiang, Anmin Shamsollahi, Golnoosh Amor, Rumelo Lanoue, Vanessa Padmanabhan, Pranesh Meunier, Frédéric A. |
author_facet | Wang, Tong Li, Wei Martin, Sally Papadopulos, Andreas Joensuu, Merja Liu, Chunxia Jiang, Anmin Shamsollahi, Golnoosh Amor, Rumelo Lanoue, Vanessa Padmanabhan, Pranesh Meunier, Frédéric A. |
author_sort | Wang, Tong |
collection | PubMed |
description | Most mammalian neurons have a narrow axon, which constrains the passage of large cargoes such as autophagosomes that can be larger than the axon diameter. Radial axonal expansion must therefore occur to ensure efficient axonal trafficking. In this study, we reveal that the speed of various large cargoes undergoing axonal transport is significantly slower than that of small ones and that the transit of diverse-sized cargoes causes an acute, albeit transient, axonal radial expansion, which is immediately restored by constitutive axonal contractility. Using live super-resolution microscopy, we demonstrate that actomyosin-II controls axonal radial contractility and local expansion, and that NM-II filaments associate with periodic F-actin rings via their head domains. Pharmacological inhibition of NM-II activity significantly increases axon diameter by detaching the NM-II from F-actin and impacts the trafficking speed, directionality, and overall efficiency of long-range retrograde trafficking. Consequently, prolonged NM-II inactivation leads to disruption of periodic actin rings and formation of focal axonal swellings, a hallmark of axonal degeneration. |
format | Online Article Text |
id | pubmed-7199852 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Rockefeller University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-71998522020-11-04 Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability Wang, Tong Li, Wei Martin, Sally Papadopulos, Andreas Joensuu, Merja Liu, Chunxia Jiang, Anmin Shamsollahi, Golnoosh Amor, Rumelo Lanoue, Vanessa Padmanabhan, Pranesh Meunier, Frédéric A. J Cell Biol Article Most mammalian neurons have a narrow axon, which constrains the passage of large cargoes such as autophagosomes that can be larger than the axon diameter. Radial axonal expansion must therefore occur to ensure efficient axonal trafficking. In this study, we reveal that the speed of various large cargoes undergoing axonal transport is significantly slower than that of small ones and that the transit of diverse-sized cargoes causes an acute, albeit transient, axonal radial expansion, which is immediately restored by constitutive axonal contractility. Using live super-resolution microscopy, we demonstrate that actomyosin-II controls axonal radial contractility and local expansion, and that NM-II filaments associate with periodic F-actin rings via their head domains. Pharmacological inhibition of NM-II activity significantly increases axon diameter by detaching the NM-II from F-actin and impacts the trafficking speed, directionality, and overall efficiency of long-range retrograde trafficking. Consequently, prolonged NM-II inactivation leads to disruption of periodic actin rings and formation of focal axonal swellings, a hallmark of axonal degeneration. Rockefeller University Press 2020-03-17 /pmc/articles/PMC7199852/ /pubmed/32182623 http://dx.doi.org/10.1083/jcb.201902001 Text en © 2020 Wang et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/). |
spellingShingle | Article Wang, Tong Li, Wei Martin, Sally Papadopulos, Andreas Joensuu, Merja Liu, Chunxia Jiang, Anmin Shamsollahi, Golnoosh Amor, Rumelo Lanoue, Vanessa Padmanabhan, Pranesh Meunier, Frédéric A. Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
title | Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
title_full | Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
title_fullStr | Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
title_full_unstemmed | Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
title_short | Radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
title_sort | radial contractility of actomyosin rings facilitates axonal trafficking and structural stability |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7199852/ https://www.ncbi.nlm.nih.gov/pubmed/32182623 http://dx.doi.org/10.1083/jcb.201902001 |
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