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Optic cup morphogenesis requires neural crest-mediated basement membrane assembly

Organogenesis requires precise interactions between a developing tissue and its environment. In vertebrates, the developing eye is surrounded by a complex extracellular matrix as well as multiple mesenchymal cell populations. Disruptions to either the matrix or periocular mesenchyme can cause defect...

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Detalles Bibliográficos
Autores principales: Bryan, Chase D., Casey, Macaulie A., Pfeiffer, Rebecca L., Jones, Bryan W., Kwan, Kristen M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7044464/
https://www.ncbi.nlm.nih.gov/pubmed/31988185
http://dx.doi.org/10.1242/dev.181420
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author Bryan, Chase D.
Casey, Macaulie A.
Pfeiffer, Rebecca L.
Jones, Bryan W.
Kwan, Kristen M.
author_facet Bryan, Chase D.
Casey, Macaulie A.
Pfeiffer, Rebecca L.
Jones, Bryan W.
Kwan, Kristen M.
author_sort Bryan, Chase D.
collection PubMed
description Organogenesis requires precise interactions between a developing tissue and its environment. In vertebrates, the developing eye is surrounded by a complex extracellular matrix as well as multiple mesenchymal cell populations. Disruptions to either the matrix or periocular mesenchyme can cause defects in early eye development, yet in many cases the underlying mechanism is unknown. Here, using multidimensional imaging and computational analyses in zebrafish, we establish that cell movements in the developing optic cup require neural crest. Ultrastructural analysis reveals that basement membrane formation around the developing eye is also dependent on neural crest, but only specifically around the retinal pigment epithelium. Neural crest cells produce the extracellular matrix protein nidogen: impairing nidogen function disrupts eye development, and, strikingly, expression of nidogen in the absence of neural crest partially restores optic cup morphogenesis. These results demonstrate that eye formation is regulated in part by extrinsic control of extracellular matrix assembly. This article has an associated ‘The people behind the papers’ interview.
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spelling pubmed-70444642020-03-12 Optic cup morphogenesis requires neural crest-mediated basement membrane assembly Bryan, Chase D. Casey, Macaulie A. Pfeiffer, Rebecca L. Jones, Bryan W. Kwan, Kristen M. Development Research Article Organogenesis requires precise interactions between a developing tissue and its environment. In vertebrates, the developing eye is surrounded by a complex extracellular matrix as well as multiple mesenchymal cell populations. Disruptions to either the matrix or periocular mesenchyme can cause defects in early eye development, yet in many cases the underlying mechanism is unknown. Here, using multidimensional imaging and computational analyses in zebrafish, we establish that cell movements in the developing optic cup require neural crest. Ultrastructural analysis reveals that basement membrane formation around the developing eye is also dependent on neural crest, but only specifically around the retinal pigment epithelium. Neural crest cells produce the extracellular matrix protein nidogen: impairing nidogen function disrupts eye development, and, strikingly, expression of nidogen in the absence of neural crest partially restores optic cup morphogenesis. These results demonstrate that eye formation is regulated in part by extrinsic control of extracellular matrix assembly. This article has an associated ‘The people behind the papers’ interview. The Company of Biologists Ltd 2020-02-21 /pmc/articles/PMC7044464/ /pubmed/31988185 http://dx.doi.org/10.1242/dev.181420 Text en © 2020. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/4.0This 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
Bryan, Chase D.
Casey, Macaulie A.
Pfeiffer, Rebecca L.
Jones, Bryan W.
Kwan, Kristen M.
Optic cup morphogenesis requires neural crest-mediated basement membrane assembly
title Optic cup morphogenesis requires neural crest-mediated basement membrane assembly
title_full Optic cup morphogenesis requires neural crest-mediated basement membrane assembly
title_fullStr Optic cup morphogenesis requires neural crest-mediated basement membrane assembly
title_full_unstemmed Optic cup morphogenesis requires neural crest-mediated basement membrane assembly
title_short Optic cup morphogenesis requires neural crest-mediated basement membrane assembly
title_sort optic cup morphogenesis requires neural crest-mediated basement membrane assembly
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7044464/
https://www.ncbi.nlm.nih.gov/pubmed/31988185
http://dx.doi.org/10.1242/dev.181420
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