Open AccessEpithelial organ shape is generated by patterned actomyosin contractility and maintained by the extracellular matrix
Author(s) -
Ali Nematbakhsh,
Megan Levis,
Nilay Kumar,
Weitao Chen,
Jeremiah J. Zartman,
Mark Alber
Publication year - 2020
Publication title -
plos computational biology/plos computational biology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 2.628
H-Index - 182
eISSN - 1553-7358
pISSN - 1553-734X
DOI - 10.1371/journal.pcbi.1008105
Subject(s) - extracellular matrix , contractility , microbiology and biotechnology , focal adhesion , actin , imaginal disc , matrix (chemical analysis) , biophysics , tension (geology) , biology , chemistry , anatomy , phenotype , materials science , biochemistry , phosphorylation , chromatography , endocrinology , ultimate tensile strength , gene , metallurgy
Epithelial sheets define organ architecture during development. Here, we employed an iterative multiscale computational modeling and quantitative experimental approach to decouple direct and indirect effects of actomyosin-generated forces, nuclear positioning, extracellular matrix, and cell-cell adhesion in shaping Drosophila wing imaginal discs. Basally generated actomyosin forces generate epithelial bending of the wing disc pouch. Surprisingly, acute pharmacological inhibition of ROCK-driven actomyosin contractility does not impact the maintenance of tissue height or curved shape. Computational simulations show that ECM tautness provides only a minor contribution to modulating tissue shape. Instead, passive ECM pre-strain serves to maintain the shape independent from actomyosin contractility. These results provide general insight into how the subcellular forces are generated and maintained within individual cells to induce tissue curvature. Thus, the results suggest an important design principle of separable contributions from ECM prestrain and actomyosin tension during epithelial organogenesis and homeostasis.