Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis

Organ formation is a multi-scale event that involves changes at the intracellular, cellular and tissue level. Organogenesis often starts with the formation of characteristically shaped organ precursors. However, the cellular mechanisms driving organ precursor formation are often not clear. Here, usi...

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Main Authors: Jaydeep Sidhaye, Caren Norden
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/22689
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author Jaydeep Sidhaye
Caren Norden
author_facet Jaydeep Sidhaye
Caren Norden
author_sort Jaydeep Sidhaye
collection DOAJ
description Organ formation is a multi-scale event that involves changes at the intracellular, cellular and tissue level. Organogenesis often starts with the formation of characteristically shaped organ precursors. However, the cellular mechanisms driving organ precursor formation are often not clear. Here, using zebrafish, we investigate the epithelial rearrangements responsible for the development of the hemispherical retinal neuroepithelium (RNE), a part of the optic cup. We show that in addition to basal shrinkage of RNE cells, active migration of connected epithelial cells into the RNE is a crucial player in its formation. This cellular movement is driven by progressive cell-matrix contacts and actively translocates prospective RNE cells to their correct location before they adopt neuroepithelial fate. Failure of this migration during neuroepithelium formation leads to ectopic determination of RNE cells and consequently impairs optic cup formation. Overall, this study illustrates how spatiotemporal coordination between morphogenic movements and fate determination critically influences organogenesis.
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spelling doaj.art-e12265092fb14138a1ea791e2ad50a962022-12-22T02:05:03ZengeLife Sciences Publications LtdeLife2050-084X2017-04-01610.7554/eLife.22689Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesisJaydeep Sidhaye0https://orcid.org/0000-0001-7858-8105Caren Norden1https://orcid.org/0000-0001-8835-1451Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Dresden International Graduate School for Biomedicine and Bioengineering, Technische Universität Dresden, Dresden, GermanyMax Planck Institute of Molecular Cell Biology and Genetics, Dresden, GermanyOrgan formation is a multi-scale event that involves changes at the intracellular, cellular and tissue level. Organogenesis often starts with the formation of characteristically shaped organ precursors. However, the cellular mechanisms driving organ precursor formation are often not clear. Here, using zebrafish, we investigate the epithelial rearrangements responsible for the development of the hemispherical retinal neuroepithelium (RNE), a part of the optic cup. We show that in addition to basal shrinkage of RNE cells, active migration of connected epithelial cells into the RNE is a crucial player in its formation. This cellular movement is driven by progressive cell-matrix contacts and actively translocates prospective RNE cells to their correct location before they adopt neuroepithelial fate. Failure of this migration during neuroepithelium formation leads to ectopic determination of RNE cells and consequently impairs optic cup formation. Overall, this study illustrates how spatiotemporal coordination between morphogenic movements and fate determination critically influences organogenesis.https://elifesciences.org/articles/22689epithelial morphogenesisretinal neuroepitheliumcollective cell migrationepithelial invagination
spellingShingle Jaydeep Sidhaye
Caren Norden
Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
eLife
epithelial morphogenesis
retinal neuroepithelium
collective cell migration
epithelial invagination
title Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
title_full Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
title_fullStr Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
title_full_unstemmed Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
title_short Concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
title_sort concerted action of neuroepithelial basal shrinkage and active epithelial migration ensures efficient optic cup morphogenesis
topic epithelial morphogenesis
retinal neuroepithelium
collective cell migration
epithelial invagination
url https://elifesciences.org/articles/22689
work_keys_str_mv AT jaydeepsidhaye concertedactionofneuroepithelialbasalshrinkageandactiveepithelialmigrationensuresefficientopticcupmorphogenesis
AT carennorden concertedactionofneuroepithelialbasalshrinkageandactiveepithelialmigrationensuresefficientopticcupmorphogenesis