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Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons
BACKGROUND: During brain development, neurons migrate from germinal zones to their final positions to assemble neural circuits. A unique saltatory cadence involving cyclical organelle movement (e.g., centrosome motility) and leading-process actomyosin enrichment prior to nucleokinesis organizes neur...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4289176/ https://www.ncbi.nlm.nih.gov/pubmed/25467954 http://dx.doi.org/10.1186/1749-8104-9-26 |
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author | Trivedi, Niraj Ramahi, Joseph S Karakaya, Mahmut Howell, Danielle Kerekes, Ryan A Solecki, David J |
author_facet | Trivedi, Niraj Ramahi, Joseph S Karakaya, Mahmut Howell, Danielle Kerekes, Ryan A Solecki, David J |
author_sort | Trivedi, Niraj |
collection | PubMed |
description | BACKGROUND: During brain development, neurons migrate from germinal zones to their final positions to assemble neural circuits. A unique saltatory cadence involving cyclical organelle movement (e.g., centrosome motility) and leading-process actomyosin enrichment prior to nucleokinesis organizes neuronal migration. While functional evidence suggests that leading-process actomyosin is essential for centrosome motility, the role of the actin-enriched leading process in globally organizing organelle transport or traction forces remains unexplored. RESULTS: We show that myosin ii motors and F-actin dynamics are required for Golgi apparatus positioning before nucleokinesis in cerebellar granule neurons (CGNs) migrating along glial fibers. Moreover, we show that primary cilia are motile organelles, localized to the leading-process F-actin-rich domain and immobilized by pharmacological inhibition of myosin ii and F-actin dynamics. Finally, leading process adhesion dynamics are dependent on myosin ii and F-actin. CONCLUSIONS: We propose that actomyosin coordinates the overall polarity of migrating CGNs by controlling asymmetric organelle positioning and cell-cell contacts as these cells move along their glial guides. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1749-8104-9-26) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4289176 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-42891762015-01-11 Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons Trivedi, Niraj Ramahi, Joseph S Karakaya, Mahmut Howell, Danielle Kerekes, Ryan A Solecki, David J Neural Dev Research Article BACKGROUND: During brain development, neurons migrate from germinal zones to their final positions to assemble neural circuits. A unique saltatory cadence involving cyclical organelle movement (e.g., centrosome motility) and leading-process actomyosin enrichment prior to nucleokinesis organizes neuronal migration. While functional evidence suggests that leading-process actomyosin is essential for centrosome motility, the role of the actin-enriched leading process in globally organizing organelle transport or traction forces remains unexplored. RESULTS: We show that myosin ii motors and F-actin dynamics are required for Golgi apparatus positioning before nucleokinesis in cerebellar granule neurons (CGNs) migrating along glial fibers. Moreover, we show that primary cilia are motile organelles, localized to the leading-process F-actin-rich domain and immobilized by pharmacological inhibition of myosin ii and F-actin dynamics. Finally, leading process adhesion dynamics are dependent on myosin ii and F-actin. CONCLUSIONS: We propose that actomyosin coordinates the overall polarity of migrating CGNs by controlling asymmetric organelle positioning and cell-cell contacts as these cells move along their glial guides. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1749-8104-9-26) contains supplementary material, which is available to authorized users. BioMed Central 2014-12-02 /pmc/articles/PMC4289176/ /pubmed/25467954 http://dx.doi.org/10.1186/1749-8104-9-26 Text en © Trivedi et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Trivedi, Niraj Ramahi, Joseph S Karakaya, Mahmut Howell, Danielle Kerekes, Ryan A Solecki, David J Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
title | Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
title_full | Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
title_fullStr | Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
title_full_unstemmed | Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
title_short | Leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
title_sort | leading-process actomyosin coordinates organelle positioning and adhesion receptor dynamics in radially migrating cerebellar granule neurons |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4289176/ https://www.ncbi.nlm.nih.gov/pubmed/25467954 http://dx.doi.org/10.1186/1749-8104-9-26 |
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