Tissue-scale mechanical coupling reduces morphogenetic noise to ensure precision during epithelial folding

Morphological constancy is universal in developing systems. It is unclear whether precise morphogenesis stems from faithful mechanical interpretation of gene expression patterns. We investigate the formation of the cephalic furrow, an epithelial fold that is precisely positioned with a linear morpho...

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Main Authors: Eritano, Anthony (Author) , Bromley, Claire L. (Author) , Bolea Albero, Antonio (Author) , Schütz, Lucas (Author) , Wen, Fu-Lai (Author) , Takeda, Michiko (Author) , Fukaya, Takashi (Author) , Sami, Mustafa M. (Author) , Shibata, Tatsuo (Author) , Lemke, Steffen (Author) , Wang, Yu-Chiun (Author)
Format: Article (Journal)
Language:English
Published: March 12, 2020
In: Developmental cell
Year: 2020, Volume: 53, Issue: 2, Pages: 212-228.e1-e12
ISSN:1878-1551
DOI:10.1016/j.devcel.2020.02.012
Online Access:Verlag, lizenzpflichtig, Volltext: https://doi.org/10.1016/j.devcel.2020.02.012
Verlag, lizenzpflichtig, Volltext: http://www.sciencedirect.com/science/article/pii/S1534580720301088
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Author Notes:Anthony S. Eritano, Claire L. Bromley, Antonio Bolea Albero, Lucas Schütz, Fu-Lai Wen, Michiko Takeda, Takashi Fukaya, Mustafa M. Sami, Tatsuo Shibata, Steffen Lemke, and Yu-Chiun Wang
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Summary:Morphological constancy is universal in developing systems. It is unclear whether precise morphogenesis stems from faithful mechanical interpretation of gene expression patterns. We investigate the formation of the cephalic furrow, an epithelial fold that is precisely positioned with a linear morphology. Fold initiation is specified by a precise genetic code with single-cell row resolution. This positional code activates and spatially confines lateral myosin contractility to induce folding. However, 20% of initiating cells are mis-specified because of fluctuating myosin intensities at the cellular level. Nevertheless, the furrow remains linearly aligned. We find that lateral myosin is planar polarized, integrating contractile membrane interfaces into supracellular “ribbons.” Local reduction of mechanical coupling at the “ribbons” using optogenetics decreases furrow linearity. Furthermore, 3D vertex modeling indicates that polarized, interconnected contractility confers morphological robustness against noise. Thus, tissue-scale mechanical coupling functions as a denoising mechanism to ensure morphogenetic precision despite noisy decoding of positional information.
Item Description:Gesehen am 14.05.2020
Physical Description:Online Resource
ISSN:1878-1551
DOI:10.1016/j.devcel.2020.02.012