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A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis

Dynamic contacts between cells within the developing neuroepithelium are poorly understood but play important roles in cell and tissue morphology and cell signalling. Here, using live-cell imaging and electron microscopy we reveal multiple protrusive structures in neuroepithelial apical endfeet of t...

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Autores principales: Kasioulis, Ioannis, Dady, Alwyn, James, John, Prescott, Alan, Halley, Pamela A., Storey, Kate G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8995095/
https://www.ncbi.nlm.nih.gov/pubmed/35217862
http://dx.doi.org/10.1242/jcs.259897
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author Kasioulis, Ioannis
Dady, Alwyn
James, John
Prescott, Alan
Halley, Pamela A.
Storey, Kate G.
author_facet Kasioulis, Ioannis
Dady, Alwyn
James, John
Prescott, Alan
Halley, Pamela A.
Storey, Kate G.
author_sort Kasioulis, Ioannis
collection PubMed
description Dynamic contacts between cells within the developing neuroepithelium are poorly understood but play important roles in cell and tissue morphology and cell signalling. Here, using live-cell imaging and electron microscopy we reveal multiple protrusive structures in neuroepithelial apical endfeet of the chick embryonic spinal cord, including sub-apical protrusions that extend laterally within the tissue, and observe similar structures in human neuroepithelium. We characterise the dynamics, shape and cytoskeleton of these lateral protrusions and distinguish them from cytonemes, filopodia and tunnelling nanotubes. We demonstrate that lateral protrusions form a latticework of membrane contacts between non-adjacent cells, depend on actin but not microtubule dynamics, and provide a lamellipodial-like platform for further extending fine actin-dependent filipodia. We find that lateral protrusions depend on the actin-binding protein WAVE1 (also known as WASF1): misexpression of mutant WAVE1 attenuated protrusion and generated a round-ended apical endfoot morphology. However, this did not alter apico-basal cell polarity or tissue integrity. During normal neuronal delamination, lateral protrusions were withdrawn, but precocious protrusion loss induced by mutant WAVE1 was insufficient to trigger neurogenesis. This study uncovers a new form of cell–cell contact within the developing neuroepithelium, regulation of which prefigures neuronal delamination. This article has an associated First Person interview with the first author of the paper.
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spelling pubmed-89950952022-04-25 A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis Kasioulis, Ioannis Dady, Alwyn James, John Prescott, Alan Halley, Pamela A. Storey, Kate G. J Cell Sci Research Article Dynamic contacts between cells within the developing neuroepithelium are poorly understood but play important roles in cell and tissue morphology and cell signalling. Here, using live-cell imaging and electron microscopy we reveal multiple protrusive structures in neuroepithelial apical endfeet of the chick embryonic spinal cord, including sub-apical protrusions that extend laterally within the tissue, and observe similar structures in human neuroepithelium. We characterise the dynamics, shape and cytoskeleton of these lateral protrusions and distinguish them from cytonemes, filopodia and tunnelling nanotubes. We demonstrate that lateral protrusions form a latticework of membrane contacts between non-adjacent cells, depend on actin but not microtubule dynamics, and provide a lamellipodial-like platform for further extending fine actin-dependent filipodia. We find that lateral protrusions depend on the actin-binding protein WAVE1 (also known as WASF1): misexpression of mutant WAVE1 attenuated protrusion and generated a round-ended apical endfoot morphology. However, this did not alter apico-basal cell polarity or tissue integrity. During normal neuronal delamination, lateral protrusions were withdrawn, but precocious protrusion loss induced by mutant WAVE1 was insufficient to trigger neurogenesis. This study uncovers a new form of cell–cell contact within the developing neuroepithelium, regulation of which prefigures neuronal delamination. This article has an associated First Person interview with the first author of the paper. The Company of Biologists Ltd 2022-03-30 /pmc/articles/PMC8995095/ /pubmed/35217862 http://dx.doi.org/10.1242/jcs.259897 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Kasioulis, Ioannis
Dady, Alwyn
James, John
Prescott, Alan
Halley, Pamela A.
Storey, Kate G.
A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
title A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
title_full A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
title_fullStr A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
title_full_unstemmed A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
title_short A lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
title_sort lateral protrusion latticework connects neuroepithelial cells and is regulated during neurogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8995095/
https://www.ncbi.nlm.nih.gov/pubmed/35217862
http://dx.doi.org/10.1242/jcs.259897
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