Cargando…

Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues

The emerging field of synthetic developmental biology proposes bottom-up approaches to examine the contribution of each cellular process to complex morphogenesis. However, the shortage of tools to manipulate three-dimensional (3D) shapes of mammalian tissues hinders the progress of the field. Here w...

Descripción completa

Detalles Bibliográficos
Autores principales: Martínez-Ara, Guillermo, Taberner, Núria, Takayama, Mami, Sandaltzopoulou, Elissavet, Villava, Casandra E., Bosch-Padrós, Miquel, Takata, Nozomu, Trepat, Xavier, Eiraku, Mototsugu, Ebisuya, Miki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9474505/
https://www.ncbi.nlm.nih.gov/pubmed/36104355
http://dx.doi.org/10.1038/s41467-022-33115-0
_version_ 1784789733503664128
author Martínez-Ara, Guillermo
Taberner, Núria
Takayama, Mami
Sandaltzopoulou, Elissavet
Villava, Casandra E.
Bosch-Padrós, Miquel
Takata, Nozomu
Trepat, Xavier
Eiraku, Mototsugu
Ebisuya, Miki
author_facet Martínez-Ara, Guillermo
Taberner, Núria
Takayama, Mami
Sandaltzopoulou, Elissavet
Villava, Casandra E.
Bosch-Padrós, Miquel
Takata, Nozomu
Trepat, Xavier
Eiraku, Mototsugu
Ebisuya, Miki
author_sort Martínez-Ara, Guillermo
collection PubMed
description The emerging field of synthetic developmental biology proposes bottom-up approaches to examine the contribution of each cellular process to complex morphogenesis. However, the shortage of tools to manipulate three-dimensional (3D) shapes of mammalian tissues hinders the progress of the field. Here we report the development of OptoShroom3, an optogenetic tool that achieves fast spatiotemporal control of apical constriction in mammalian epithelia. Activation of OptoShroom3 through illumination in an epithelial Madin-Darby Canine Kidney (MDCK) cell sheet reduces the apical surface of the stimulated cells and causes displacements in the adjacent regions. Light-induced apical constriction provokes the folding of epithelial cell colonies on soft gels. Its application to murine and human neural organoids leads to thickening of neuroepithelia, apical lumen reduction in optic vesicles, and flattening in neuroectodermal tissues. These results show that spatiotemporal control of apical constriction can trigger several types of 3D deformation depending on the initial tissue context.
format Online
Article
Text
id pubmed-9474505
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-94745052022-09-16 Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues Martínez-Ara, Guillermo Taberner, Núria Takayama, Mami Sandaltzopoulou, Elissavet Villava, Casandra E. Bosch-Padrós, Miquel Takata, Nozomu Trepat, Xavier Eiraku, Mototsugu Ebisuya, Miki Nat Commun Article The emerging field of synthetic developmental biology proposes bottom-up approaches to examine the contribution of each cellular process to complex morphogenesis. However, the shortage of tools to manipulate three-dimensional (3D) shapes of mammalian tissues hinders the progress of the field. Here we report the development of OptoShroom3, an optogenetic tool that achieves fast spatiotemporal control of apical constriction in mammalian epithelia. Activation of OptoShroom3 through illumination in an epithelial Madin-Darby Canine Kidney (MDCK) cell sheet reduces the apical surface of the stimulated cells and causes displacements in the adjacent regions. Light-induced apical constriction provokes the folding of epithelial cell colonies on soft gels. Its application to murine and human neural organoids leads to thickening of neuroepithelia, apical lumen reduction in optic vesicles, and flattening in neuroectodermal tissues. These results show that spatiotemporal control of apical constriction can trigger several types of 3D deformation depending on the initial tissue context. Nature Publishing Group UK 2022-09-14 /pmc/articles/PMC9474505/ /pubmed/36104355 http://dx.doi.org/10.1038/s41467-022-33115-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Martínez-Ara, Guillermo
Taberner, Núria
Takayama, Mami
Sandaltzopoulou, Elissavet
Villava, Casandra E.
Bosch-Padrós, Miquel
Takata, Nozomu
Trepat, Xavier
Eiraku, Mototsugu
Ebisuya, Miki
Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
title Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
title_full Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
title_fullStr Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
title_full_unstemmed Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
title_short Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
title_sort optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9474505/
https://www.ncbi.nlm.nih.gov/pubmed/36104355
http://dx.doi.org/10.1038/s41467-022-33115-0
work_keys_str_mv AT martinezaraguillermo optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT tabernernuria optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT takayamamami optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT sandaltzopoulouelissavet optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT villavacasandrae optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT boschpadrosmiquel optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT takatanozomu optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT trepatxavier optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT eirakumototsugu optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues
AT ebisuyamiki optogeneticcontrolofapicalconstrictioninducessyntheticmorphogenesisinmammaliantissues