Tissue rheology in embryonic organization

Abstract

Tissue morphogenesis in multicellular organisms is brought about by spatiotemporal coordination of mechanical and chemical signals. Extensive work on how mechanical forces together with the well‐established morphogen signalling pathways can actively shape living tissues has revealed evolutionary conserved mechanochemical features of embryonic development. More recently, attention has been drawn to the description of tissue material properties and how they can influence certain morphogenetic processes. Interestingly, besides the role of tissue material properties in determining how much tissues deform in response to force application, there is increasing theoretical and experimental evidence, suggesting that tissue material properties can abruptly and drastically change in development. These changes resemble phase transitions, pointing at the intriguing possibility that important morphogenetic processes in development, such as symmetry breaking and self‐organization, might be mediated by tissue phase transitions. In this review, we summarize recent findings on the regulation and role of tissue material properties in the context of the developing embryo. We posit that abrupt changes of tissue rheological properties may have important implications in maintaining the balance between robustness and adaptability during embryonic development.

In primary airway epithelial cells, the unjamming transition is distinct from the epithelial-to-mesenchymal transition

“…In certain contexts, however, this conversion from sedentary to migratory behavior has been attributed to the recently discovered unjamming transition (UJT), in which epithelial cells migrate collectively and cooperatively [37][38][39][40] . By contrast with EMT, UJT in epithelial tissues is recently discovered and remains poorly understood [37][38][39][40][41][42][43][44][45][46][47][48][49][50] . During UJT the epithelial collective transitions from a jammed phase wherein cells remain virtually locked in place, as if the cellular collective were frozen and solid-like, toward an unjammed phase wherein cells often migrate in cooperative multicellular packs and swirls reminiscent of fluid flow.…”

“…But as the system progressively unjams and transitions to a fluid-like phase local rearrangements amongst neighboring cells become increasingly possible and tend to be cooperative, intermittent, and heterogeneous 46,[51][52][53][54] . While poorly understood, cellular jamming and unjamming have been identified in epithelial systems in vitro 37,39,43,46,48,49,[54][55][56] , in developmental systems in vivo 39,42,50,[57][58][59] , and have been linked to the pathobiology of asthma [37][38][39] and cancer 45,47,60,61 .…”

On growth and force: mechanical forces in development

“…It has long been known that epithelia exhibit a viscoelastic behaviour (Petridou et al, 2019): while they return to their resting shape in response to a transient force of deformation, they slowly and irreversibly deform by dissipating mechanical stress in response to a more sustained mechanical stimulus. Using a combination of live imaging and optogenetics, Margaret Gardel (University of Chicago, USA) showed how irreversible deformation of epithelia can be generated by pulsatile RhoA activity via pulsatile ratchet-like shortening of intercellular contacts that relies on mechanosensitive E-cadherin endocytosis (Cavanaugh et al, 2019, Staddon et al, 2019.…”

Interplay of mesoscale physics and agent-like behaviors in the parallel evolution of aggregative multicellularity

“…Specifically, there is a recognition that the shaping of multicellular masses cannot be explained independently of their material properties, and that developing organisms are thus subject to physical forces and effects relevant to their composition and scale [ 36 – 39 ]. When applied, for example, to embryonic animal tissues, which (due to the capacity of their cellular subunits to remain cohesive while exhibiting independent motility) behave similarly in certain respects to non-living liquids, physical models predict the formation of immiscible layers, interior spaces, and, when the subunits are anisotropic, the capacity to undergo elongation [ 36 , 40 , 41 ]. In contrast, plant tissues, characterized by rigid cell walls, behave like deformable, mechanically and chemically active solids which (unlike liquid-state materials) can bud or branch [ 39 ].…”