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

Abstract

SummaryAs 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.

Tissue rheology in embryonic organization

“…Previous studies suggested that tissue viscoelasticity influences the length scale of mechanical signal propagation, such as cortical flows in C. elegans zygotes (Mayer et al, 2010), or stress-induced cell shape change propagation across the Drosophila wing imaginal disc epithelium (Duda et al, 2019). Previous studies suggested that tissue viscoelasticity influences the length scale of mechanical signal propagation, such as cortical flows in C. elegans zygotes (Mayer et al, 2010), or stress-induced cell shape change propagation across the Drosophila wing imaginal disc epithelium (Duda et al, 2019).…”

“…Another so far largely unexplored question is whether tissue rheological properties are not only controlled by mechanochemical signalling but also affect such signalling. Previous studies suggested that tissue viscoelasticity influences the length scale of mechanical signal propagation, such as cortical flows in C. elegans zygotes (Mayer et al, 2010), or stress-induced cell shape change propagation across the Drosophila wing imaginal disc epithelium (Duda et al, 2019). However, whether and how tissues displaying nonuniform rheology affect the transduction of long-range mechanical signals generated by, e.g., supra-cellular actomyosin cables (Behrndt et al, 2012;Röper, 2013;preprint: Saadaoui et al, 2018;Shook et al, 2018) remains unclear.…”

“…While most data so far support a permissive role of tissue material properties in tissue morphogenesis (Shook et al, 2018;Duda et al, 2019;Iyer et al, 2019), recent work also suggests that developing tissues can actively undergo pronounced changes in their material properties, modulating tissue shape changes (Petridou et al, 2019) and triggering other processes, such as cell migration . In some cases, these changes can be abrupt, thereby resembling phase transitions (i.e.…”

Mechanosensitive junction remodelling promotes robust epithelial morphogenesis

“…(9)] and thresholded tension remodelling [Eq. (10)] is sufficient to capture the experimentally observed mechanical behaviour of epithelial junctions, as well as ratcheted contractions upon episodic activation of contractility. In agreement with experimental data (Fig 2d), the junction shrinks to ∼ 80% of its initial length after the first contraction, while after the second contraction pulse, the normalised junction length is 70%, roughly 85% of its length after the first pulse (Fig 4c).…”

“…A number of different experimental techniques and model systems have been used to probe the viscoelastic properties of epithelial cells. Rheological studies on suspended epithelial monolayers [8] have shown that stress dissipation in strained tissues is controlled by cell divisions, or actomyosin turnover [9,10]. Optical tweezers have been used to probe the mechanical response of cell-cell junctions under short time scale forces, where they respond elastically [6].…”