Polarization of Myosin II Refines Tissue Material Properties to Buffer Mechanical Stress

As tissues develop, they are subjected to a variety of mechanical forces. Some of these forces are instrumental in the development of tissues, while others can result in tissue damage. Despite our extensive understanding of force-guided morphogenesis, we have only a limited understanding of how tissues prevent further morphogenesis once the shape is determined after development. Here, through the development of a tissue-stretching device, we uncover a mechanosensitive pathway that regulates tissue responses to mechanical stress through the polarization of actomyosin across the tissue. We show that stretch induces the formation of linear multicellular actomyosin cables, which depend on Diaphanous for their nucleation. These stiffen the epithelium, limiting further changes in shape, and prevent fractures from propagating across the tissue. Overall, this mechanism of force-induced changes in tissue mechanical properties provides a general model of force buffering that serves to preserve the shape of tissues under conditions of mechanical stress. [Display omitted] •MyoII forms polarized cables upon mechanical stretch•MyoII polarity increases tissue stiffness and elasticity in the direction of stretch•MyoII cables protect tissues from fluctuations in forces to maintain tissue shape•MyoII polarization is Rok-independent but mediated by actin polymerization via Dia Duda and Kirkland et al. develop a tissue-stretching device and demonstrate that Myosin II polarizes with mechanical stretch, a rapid reaction that changes tissue stiffness and elasticity to protect it from physical damage and maintain tissue shape. MyoII polarization is mediated downstream of actin polymerization via Diaphanous.