Direct laser manipulation reveals the mechanics of cell contacts in vivo

TLDR

Cell-generated forces at cytoskeletal contacts drive tissue movements and shape changes, yet the mechanical basis of these cell shape changes remains largely unknown because in vivo measurements are lacking. The study develops an optical tweezers–light-sheet microscopy approach to probe mechanical properties of epithelial cell junctions in the early Drosophila embryo. The method uses optical tweezers to deform cell‑cell interfaces while simultaneously imaging with light‑sheet microscopy to measure junctional tension. Optical trapping revealed junctional tensions of ~100 pN that equilibrate within seconds, increase and become anisotropic during morphogenesis, and fit a viscoelastic model whose constitutive law predicts how local deformations propagate across the tissue.

Abstract

Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell-cell and cell-ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell-cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue.