» Articles » PMID: 36104355

Optogenetic Control of Apical Constriction Induces Synthetic Morphogenesis in Mammalian Tissues

Overview
Journal Nat Commun
Specialty Biology
Date 2022 Sep 14
PMID 36104355
Authors
Affiliations
Soon will be listed here.
Abstract

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.

Citing Articles

Measuring and manipulating mechanical forces during development.

Villeneuve C, McCreery K, Wickstrom S Nat Cell Biol. 2025; .

PMID: 40065147 DOI: 10.1038/s41556-025-01632-x.


Designer mammalian living materials through genetic engineering.

Gameiro M, Almeida-Pinto J, Moura B, Mano J, Gaspar V Bioact Mater. 2025; 48:135-148.

PMID: 40034809 PMC: 11872553. DOI: 10.1016/j.bioactmat.2025.02.007.


The dynamics of tubulogenesis in development and disease.

Romero A, Walker B, Krneta-Stankic V, Gerner-Mauro K, Youmans L, Miller R Development. 2025; 152(3).

PMID: 39959988 PMC: 11883272. DOI: 10.1242/dev.202820.


Genetically-stable engineered optogenetic gene switches modulate spatial cell morphogenesis in two- and three-dimensional tissue cultures.

Beyer H, Kumar S, Nieke M, Diehl C, Tang K, Shumka S Nat Commun. 2024; 15(1):10470.

PMID: 39622829 PMC: 11612184. DOI: 10.1038/s41467-024-54350-7.


Image-guided optogenetic spatiotemporal tissue patterning using μPatternScope.

Kumar S, Beyer H, Chen M, Zurbriggen M, Khammash M Nat Commun. 2024; 15(1):10469.

PMID: 39622799 PMC: 11612157. DOI: 10.1038/s41467-024-54351-6.


References
1.
Hildebrand J, Soriano P . Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell. 1999; 99(5):485-97. DOI: 10.1016/s0092-8674(00)81537-8. View

2.
Ruijgrok P, Ghosh R, Zemsky S, Nakamura M, Gong R, Ning L . Optical control of fast and processive engineered myosins in vitro and in living cells. Nat Chem Biol. 2021; 17(5):540-548. PMC: 10807509. DOI: 10.1038/s41589-021-00740-7. View

3.
Campas O . A toolbox to explore the mechanics of living embryonic tissues. Semin Cell Dev Biol. 2016; 55:119-30. PMC: 4903887. DOI: 10.1016/j.semcdb.2016.03.011. View

4.
Guntas G, Hallett R, Zimmerman S, Williams T, Yumerefendi H, Bear J . Engineering an improved light-induced dimer (iLID) for controlling the localization and activity of signaling proteins. Proc Natl Acad Sci U S A. 2014; 112(1):112-7. PMC: 4291625. DOI: 10.1073/pnas.1417910112. View

5.
Barbier de Reuille P, Routier-Kierzkowska A, Kierzkowski D, Bassel G, Schupbach T, Tauriello G . MorphoGraphX: A platform for quantifying morphogenesis in 4D. Elife. 2015; 4:05864. PMC: 4421794. DOI: 10.7554/eLife.05864. View