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Microtubule-associated protein 1b is required for shaping the neural tube

BACKGROUND: Shaping of the neural tube, the precursor of the brain and spinal cord, involves narrowing and elongation of the neural tissue, concomitantly with other morphogenetic changes that contribue to this process. In zebrafish, medial displacement of neural cells (neural convergence or NC), whi...

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Autores principales: Jayachandran, Pradeepa, Olmo, Valerie N., Sanchez, Stephanie P., McFarland, Rebecca J., Vital, Eudorah, Werner, Jonathan M., Hong, Elim, Sanchez-Alberola, Neus, Molodstov, Aleksey, Brewster, Rachel M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4717579/
https://www.ncbi.nlm.nih.gov/pubmed/26782621
http://dx.doi.org/10.1186/s13064-015-0056-4
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author Jayachandran, Pradeepa
Olmo, Valerie N.
Sanchez, Stephanie P.
McFarland, Rebecca J.
Vital, Eudorah
Werner, Jonathan M.
Hong, Elim
Sanchez-Alberola, Neus
Molodstov, Aleksey
Brewster, Rachel M.
author_facet Jayachandran, Pradeepa
Olmo, Valerie N.
Sanchez, Stephanie P.
McFarland, Rebecca J.
Vital, Eudorah
Werner, Jonathan M.
Hong, Elim
Sanchez-Alberola, Neus
Molodstov, Aleksey
Brewster, Rachel M.
author_sort Jayachandran, Pradeepa
collection PubMed
description BACKGROUND: Shaping of the neural tube, the precursor of the brain and spinal cord, involves narrowing and elongation of the neural tissue, concomitantly with other morphogenetic changes that contribue to this process. In zebrafish, medial displacement of neural cells (neural convergence or NC), which drives the infolding and narrowing of the neural ectoderm, is mediated by polarized migration and cell elongation towards the dorsal midline. Failure to undergo proper NC results in severe neural tube defects, yet the molecular underpinnings of this process remain poorly understood. RESULTS: We investigated here the role of the microtubule (MT) cytoskeleton in mediating NC in zebrafish embryos using the MT destabilizing and hyperstabilizing drugs nocodazole and paclitaxel respectively. We found that MTs undergo major changes in organization and stability during neurulation and are required for the timely completion of NC by promoting cell elongation and polarity. We next examined the role of Microtubule-associated protein 1B (Map1b), previously shown to promote MT dynamicity in axons. map1b is expressed earlier than previously reported, in the developing neural tube and underlying mesoderm. Loss of Map1b function using morpholinos (MOs) or δMap1b (encoding a truncated Map1b protein product) resulted in delayed NC and duplication of the neural tube, a defect associated with impaired NC. We observed a loss of stable MTs in these embryos that is likely to contribute to the NC defect. Lastly, we found that Map1b mediates cell elongation in a cell autonomous manner and polarized protrusive activity, two cell behaviors that underlie NC and are MT-dependent. CONCLUSIONS: Together, these data highlight the importance of MTs in the early morphogenetic movements that shape the neural tube and reveal a novel role for the MT regulator Map1b in mediating cell elongation and polarized cell movement in neural progenitor cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13064-015-0056-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-47175792016-01-20 Microtubule-associated protein 1b is required for shaping the neural tube Jayachandran, Pradeepa Olmo, Valerie N. Sanchez, Stephanie P. McFarland, Rebecca J. Vital, Eudorah Werner, Jonathan M. Hong, Elim Sanchez-Alberola, Neus Molodstov, Aleksey Brewster, Rachel M. Neural Dev Research Article BACKGROUND: Shaping of the neural tube, the precursor of the brain and spinal cord, involves narrowing and elongation of the neural tissue, concomitantly with other morphogenetic changes that contribue to this process. In zebrafish, medial displacement of neural cells (neural convergence or NC), which drives the infolding and narrowing of the neural ectoderm, is mediated by polarized migration and cell elongation towards the dorsal midline. Failure to undergo proper NC results in severe neural tube defects, yet the molecular underpinnings of this process remain poorly understood. RESULTS: We investigated here the role of the microtubule (MT) cytoskeleton in mediating NC in zebrafish embryos using the MT destabilizing and hyperstabilizing drugs nocodazole and paclitaxel respectively. We found that MTs undergo major changes in organization and stability during neurulation and are required for the timely completion of NC by promoting cell elongation and polarity. We next examined the role of Microtubule-associated protein 1B (Map1b), previously shown to promote MT dynamicity in axons. map1b is expressed earlier than previously reported, in the developing neural tube and underlying mesoderm. Loss of Map1b function using morpholinos (MOs) or δMap1b (encoding a truncated Map1b protein product) resulted in delayed NC and duplication of the neural tube, a defect associated with impaired NC. We observed a loss of stable MTs in these embryos that is likely to contribute to the NC defect. Lastly, we found that Map1b mediates cell elongation in a cell autonomous manner and polarized protrusive activity, two cell behaviors that underlie NC and are MT-dependent. CONCLUSIONS: Together, these data highlight the importance of MTs in the early morphogenetic movements that shape the neural tube and reveal a novel role for the MT regulator Map1b in mediating cell elongation and polarized cell movement in neural progenitor cells. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13064-015-0056-4) contains supplementary material, which is available to authorized users. BioMed Central 2016-01-18 /pmc/articles/PMC4717579/ /pubmed/26782621 http://dx.doi.org/10.1186/s13064-015-0056-4 Text en © Jayachandran et al. 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Jayachandran, Pradeepa
Olmo, Valerie N.
Sanchez, Stephanie P.
McFarland, Rebecca J.
Vital, Eudorah
Werner, Jonathan M.
Hong, Elim
Sanchez-Alberola, Neus
Molodstov, Aleksey
Brewster, Rachel M.
Microtubule-associated protein 1b is required for shaping the neural tube
title Microtubule-associated protein 1b is required for shaping the neural tube
title_full Microtubule-associated protein 1b is required for shaping the neural tube
title_fullStr Microtubule-associated protein 1b is required for shaping the neural tube
title_full_unstemmed Microtubule-associated protein 1b is required for shaping the neural tube
title_short Microtubule-associated protein 1b is required for shaping the neural tube
title_sort microtubule-associated protein 1b is required for shaping the neural tube
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4717579/
https://www.ncbi.nlm.nih.gov/pubmed/26782621
http://dx.doi.org/10.1186/s13064-015-0056-4
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