Basal Cell-Extracellular Matrix Adhesion Regulates Force Transmission during Tissue Morphogenesis

• Published in: Developmental cell 2016-12, Vol.39 (5), p.611-625
• Main Authors: Goodwin, Katharine, Ellis, Stephanie J., Lostchuck, Emily, Zulueta-Coarasa, Teresa, Fernandez-Gonzalez, Rodrigo, Tanentzapf, Guy
• Format: Article
• Language: English
• Subjects: Animals; Animals, Genetically Modified; Biophysical Phenomena; Cell Adhesion - physiology; cell-ECM adhesion; dorsal closure; Drosophila; Drosophila - cytology; Drosophila - embryology; Drosophila - physiology; Drosophila Proteins - physiology; Extracellular Matrix - physiology; focal adhesions; Focal Adhesions - physiology; integrins; Integrins - physiology; Models, Biological; morphogenesis; Morphogenesis - physiology; tissue mechanics
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2016.11.003

Tissue morphogenesis requires force-generating mechanisms to organize cells into complex structures. Although many such mechanisms have been characterized, we know little about how forces are integrated across developing tissues. We provide evidence that integrin-mediated cell-extracellular matrix (ECM) adhesion modulates the transmission of apically generated tension during dorsal closure (DC) in Drosophila. Integrin-containing adhesive structures resembling focal adhesions were identified on the basal surface of the amnioserosa (AS), an extraembryonic epithelium essential for DC. Genetic modulation of integrin-mediated adhesion results in defective DC. Quantitative image analysis and laser ablation experiments reveal that basal cell-ECM adhesions provide resistance to apical cell displacements and force transmission between neighboring cells in the AS. Finally, we provide evidence for integrin-dependent force transmission to the AS substrate. Overall, we find that integrins regulate force transmission within and between cells, thereby playing an essential role in transmitting tension in developing tissues. [Display omitted] •Focal adhesion-like structures form on the basal surface of amnioserosa (AS) cells•Disruptions to cell-ECM adhesion affect cell deformation and impede dorsal closure•The amount of basal adhesion is inversely correlated with apical force transmission•Integrin-dependent mechanical coupling exists between AS cells and their substrate Goodwin, Ellis et al. identify integrin-containing focal adhesion-like structures on the basal amnioserosa surface that act as tethers, anchoring the apical cell surface to the substrate. These basal adhesions are required for dorsal closure, where they modulate apical surface force transmission and may resist large-scale cell displacements during tissue contraction.