Image-based parameter inference for epithelial mechanics.

Measuring mechanical parameters in tissues, such as the elastic modulus of cell-cell junctions, is essential to decipher the mechanical control of morphogenesis. However, their in vivo measurement is technically challenging. Here, we formulated an image-based statistical approach to estimate the mec...

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Main Authors: Goshi Ogita, Takefumi Kondo, Keisuke Ikawa, Tadashi Uemura, Shuji Ishihara, Kaoru Sugimura
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-06-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1010209
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author Goshi Ogita
Takefumi Kondo
Keisuke Ikawa
Tadashi Uemura
Shuji Ishihara
Kaoru Sugimura
author_facet Goshi Ogita
Takefumi Kondo
Keisuke Ikawa
Tadashi Uemura
Shuji Ishihara
Kaoru Sugimura
author_sort Goshi Ogita
collection DOAJ
description Measuring mechanical parameters in tissues, such as the elastic modulus of cell-cell junctions, is essential to decipher the mechanical control of morphogenesis. However, their in vivo measurement is technically challenging. Here, we formulated an image-based statistical approach to estimate the mechanical parameters of epithelial cells. Candidate mechanical models are constructed based on force-cell shape correlations obtained from image data. Substitution of the model functions into force-balance equations at the cell vertex leads to an equation with respect to the parameters of the model, by which one can estimate the parameter values using a least-squares method. A test using synthetic data confirmed the accuracy of parameter estimation and model selection. By applying this method to Drosophila epithelial tissues, we found that the magnitude and orientation of feedback between the junction tension and shrinkage, which are determined by the spring constant of the junction, were correlated with the elevation of tension and myosin-II on shrinking junctions during cell rearrangement. Further, this method clarified how alterations in tissue polarity and stretching affect the anisotropy in tension parameters. Thus, our method provides a novel approach to uncovering the mechanisms governing epithelial morphogenesis.
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spelling doaj.art-def01b1efa5f4614803acf89158848692022-12-22T02:31:04ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-06-01186e101020910.1371/journal.pcbi.1010209Image-based parameter inference for epithelial mechanics.Goshi OgitaTakefumi KondoKeisuke IkawaTadashi UemuraShuji IshiharaKaoru SugimuraMeasuring mechanical parameters in tissues, such as the elastic modulus of cell-cell junctions, is essential to decipher the mechanical control of morphogenesis. However, their in vivo measurement is technically challenging. Here, we formulated an image-based statistical approach to estimate the mechanical parameters of epithelial cells. Candidate mechanical models are constructed based on force-cell shape correlations obtained from image data. Substitution of the model functions into force-balance equations at the cell vertex leads to an equation with respect to the parameters of the model, by which one can estimate the parameter values using a least-squares method. A test using synthetic data confirmed the accuracy of parameter estimation and model selection. By applying this method to Drosophila epithelial tissues, we found that the magnitude and orientation of feedback between the junction tension and shrinkage, which are determined by the spring constant of the junction, were correlated with the elevation of tension and myosin-II on shrinking junctions during cell rearrangement. Further, this method clarified how alterations in tissue polarity and stretching affect the anisotropy in tension parameters. Thus, our method provides a novel approach to uncovering the mechanisms governing epithelial morphogenesis.https://doi.org/10.1371/journal.pcbi.1010209
spellingShingle Goshi Ogita
Takefumi Kondo
Keisuke Ikawa
Tadashi Uemura
Shuji Ishihara
Kaoru Sugimura
Image-based parameter inference for epithelial mechanics.
PLoS Computational Biology
title Image-based parameter inference for epithelial mechanics.
title_full Image-based parameter inference for epithelial mechanics.
title_fullStr Image-based parameter inference for epithelial mechanics.
title_full_unstemmed Image-based parameter inference for epithelial mechanics.
title_short Image-based parameter inference for epithelial mechanics.
title_sort image based parameter inference for epithelial mechanics
url https://doi.org/10.1371/journal.pcbi.1010209
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AT shujiishihara imagebasedparameterinferenceforepithelialmechanics
AT kaorusugimura imagebasedparameterinferenceforepithelialmechanics