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Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry

Neuroepithelial cells balance tissue growth requirement with the morphogenetic imperative of closing the neural tube. They apically constrict to generate mechanical forces which elevate the neural folds, but are thought to apically dilate during mitosis. However, we previously reported that mitotic...

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Autores principales: Ampartzidis, Ioakeim, Efstathiou, Christoforos, Paonessa, Francesco, Thompson, Elliott M., Wilson, Tyler, McCann, Conor J., Greene, Nicholas DE., Copp, Andrew J., Livesey, Frederick J., Elvassore, Nicola, Giobbe, Giovanni G., De Coppi, Paolo, Maniou, Eirini, Galea, Gabriel L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10570144/
https://www.ncbi.nlm.nih.gov/pubmed/36509125
http://dx.doi.org/10.1016/j.ydbio.2022.12.002
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author Ampartzidis, Ioakeim
Efstathiou, Christoforos
Paonessa, Francesco
Thompson, Elliott M.
Wilson, Tyler
McCann, Conor J.
Greene, Nicholas DE.
Copp, Andrew J.
Livesey, Frederick J.
Elvassore, Nicola
Giobbe, Giovanni G.
De Coppi, Paolo
Maniou, Eirini
Galea, Gabriel L.
author_facet Ampartzidis, Ioakeim
Efstathiou, Christoforos
Paonessa, Francesco
Thompson, Elliott M.
Wilson, Tyler
McCann, Conor J.
Greene, Nicholas DE.
Copp, Andrew J.
Livesey, Frederick J.
Elvassore, Nicola
Giobbe, Giovanni G.
De Coppi, Paolo
Maniou, Eirini
Galea, Gabriel L.
author_sort Ampartzidis, Ioakeim
collection PubMed
description Neuroepithelial cells balance tissue growth requirement with the morphogenetic imperative of closing the neural tube. They apically constrict to generate mechanical forces which elevate the neural folds, but are thought to apically dilate during mitosis. However, we previously reported that mitotic neuroepithelial cells in the mouse posterior neuropore have smaller apical surfaces than non-mitotic cells. Here, we document progressive apical enrichment of non-muscle myosin-II in mitotic, but not non-mitotic, neuroepithelial cells with smaller apical areas. Live-imaging of the chick posterior neuropore confirms apical constriction synchronised with mitosis, reaching maximal constriction by anaphase, before division and re-dilation. Mitotic apical constriction amplitude is significantly greater than interphase constrictions. To investigate conservation in humans, we characterised early stages of iPSC differentiation through dual SMAD-inhibition to robustly produce pseudostratified neuroepithelia with apically enriched actomyosin. These cultured neuroepithelial cells achieve an equivalent apical area to those in mouse embryos. iPSC-derived neuroepithelial cells have large apical areas in G2 which constrict in M phase and retain this constriction in G1/S. Given that this differentiation method produces anterior neural identities, we studied the anterior neuroepithelium of the elevating mouse mid-brain neural tube. Instead of constricting, mid-brain mitotic neuroepithelial cells have larger apical areas than interphase cells. Tissue geometry differs between the apically convex early midbrain and flat posterior neuropore. Culturing human neuroepithelia on equivalently convex surfaces prevents mitotic apical constriction. Thus, neuroepithelial cells undergo high-amplitude apical constriction synchronised with cell cycle progression but the timing of their constriction if influenced by tissue geometry.
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spelling pubmed-105701442023-10-14 Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry Ampartzidis, Ioakeim Efstathiou, Christoforos Paonessa, Francesco Thompson, Elliott M. Wilson, Tyler McCann, Conor J. Greene, Nicholas DE. Copp, Andrew J. Livesey, Frederick J. Elvassore, Nicola Giobbe, Giovanni G. De Coppi, Paolo Maniou, Eirini Galea, Gabriel L. Dev Biol Article Neuroepithelial cells balance tissue growth requirement with the morphogenetic imperative of closing the neural tube. They apically constrict to generate mechanical forces which elevate the neural folds, but are thought to apically dilate during mitosis. However, we previously reported that mitotic neuroepithelial cells in the mouse posterior neuropore have smaller apical surfaces than non-mitotic cells. Here, we document progressive apical enrichment of non-muscle myosin-II in mitotic, but not non-mitotic, neuroepithelial cells with smaller apical areas. Live-imaging of the chick posterior neuropore confirms apical constriction synchronised with mitosis, reaching maximal constriction by anaphase, before division and re-dilation. Mitotic apical constriction amplitude is significantly greater than interphase constrictions. To investigate conservation in humans, we characterised early stages of iPSC differentiation through dual SMAD-inhibition to robustly produce pseudostratified neuroepithelia with apically enriched actomyosin. These cultured neuroepithelial cells achieve an equivalent apical area to those in mouse embryos. iPSC-derived neuroepithelial cells have large apical areas in G2 which constrict in M phase and retain this constriction in G1/S. Given that this differentiation method produces anterior neural identities, we studied the anterior neuroepithelium of the elevating mouse mid-brain neural tube. Instead of constricting, mid-brain mitotic neuroepithelial cells have larger apical areas than interphase cells. Tissue geometry differs between the apically convex early midbrain and flat posterior neuropore. Culturing human neuroepithelia on equivalently convex surfaces prevents mitotic apical constriction. Thus, neuroepithelial cells undergo high-amplitude apical constriction synchronised with cell cycle progression but the timing of their constriction if influenced by tissue geometry. Elsevier 2023-02 /pmc/articles/PMC10570144/ /pubmed/36509125 http://dx.doi.org/10.1016/j.ydbio.2022.12.002 Text en © 2022 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Ampartzidis, Ioakeim
Efstathiou, Christoforos
Paonessa, Francesco
Thompson, Elliott M.
Wilson, Tyler
McCann, Conor J.
Greene, Nicholas DE.
Copp, Andrew J.
Livesey, Frederick J.
Elvassore, Nicola
Giobbe, Giovanni G.
De Coppi, Paolo
Maniou, Eirini
Galea, Gabriel L.
Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
title Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
title_full Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
title_fullStr Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
title_full_unstemmed Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
title_short Synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
title_sort synchronisation of apical constriction and cell cycle progression is a conserved behaviour of pseudostratified neuroepithelia informed by their tissue geometry
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10570144/
https://www.ncbi.nlm.nih.gov/pubmed/36509125
http://dx.doi.org/10.1016/j.ydbio.2022.12.002
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