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Armon, S.

Publications and source records attributed to Armon, S..

3 recordsLinked to original sources

Cytoskeletal networks are adaptive active elastic filamentous materials that design their own shape in response to system geometry

Living systems adopt a diversity of curved and highly dynamic shapes. These diverse morphologies appear on many length-scales, from cells to tissues and organismal scales. The common driving force for these dynamic shape changes are contractile stresses generated by myosin motors in the cell cytoskeleton, an intrinsically active filamentous material, while converting chemical energy into mechanical work. A good understanding of how contractile stresses in the cytoskeleton arise into different 3D shapes and what are the selection rules that determine their final configurations still lacks. Aiming to identify the selection rules governing the shapes formed by contractile forces in living systems, we recreate the actomyosin cytoskeleton in-vitro, with precisely controlled composition and initial geometry. A set of actomyosin gel discs, intrinsically identical but of variable initial geometry, spontaneously self-organize into a family of 3D shapes. This process occurs through robust distinct dynamical pathways, without specific pre-programming and additional regulation. Shape selection is encoded in the initial disc radius to thickness aspect ratio, and thus scale-free. This may indicate a universal process of shape selection, that works across scales, from cells to tissues and organelles. Finally, our results suggest that, while the dynamical pathways may depend on the detailed interactions of the different microscopic components within the gel, the final selected shapes obey the general theory of elastic deformations of thin sheets. Altogether, these results provide novel insights on the mechanically induced spontaneous shape transitions in active contractile matter and uncover new mechanisms that drive shape selections in living systems across scales. Significance statementLiving systems adopt a diversity of curved and highly dynamic shapes. These diverse morphologies appear on many length-scales, from cells to organismal scales, and are commonly driven by contractile stresses generated by myosin motors in the cell cytoskeleton. By recreating the actomyosin cytoskeleton in-vitro, with precisely controlled composition and initial geometry, we identify the shape selection rules that determine the final adopted configuration. Specifically, we find that shape selection is scale-free, which may indicate a universal process of shape selection, that works across scales, from cells to tissues and organelles. Altogether, our results provide novel insights on the mechanically induced spontaneous shape transitions in contractile active matter and uncover new mechanisms that drive shape selections in living systems.

biophysics↗

Epithelial Tissues as Active Solids: From Nonlinear Contraction Pulses to Rupture Resistance

Epithelial tissues in many contexts can be viewed as soft active solids. Their active nature is manifested in the ability of individual cells within the tissue to contract and/or remodel their mechanical properties in response to various conditions. Little is known about the emergent properties of such materials. Specifically, how an individual cellular activity gives rise to collective spatiotemporal patterns is not fully understood. Recently we reported the observation of ultrafast contraction pulses in the dorsal epithelium of T.adhaerens in vivo [1] and speculated these propagate via mechanical fields. Other accumulating evidence suggest mechanics is involved in similar contractile patterns in embryonic development in vivo and in cellular monolayers in vitro. Here we show that a widespread cellular response - activation of contraction in response to stretch - is sufficient to give rise to nonlinear propagating contraction pulses. Using a minimal numerical model and theoretical considerations we show how such mechanical pulses emerge and propagate, spontaneously or in response to external stretch. The model - whose mathematical structure resembles that of reaction-diffusion systems - explains observed phenomena in T. adhaerens (e.g. excitable or spontaneous pulses, pulse interaction) and predicts other phenomena (e.g. symmetric strain profile, "spike trains"). Finally, we show that in response to external tension, such an active two-dimensional sheet lowers and dynamically distributes the strains across its surface, hence facilitating tissue resistance to rupture. Adding a cellular softening-threshold further enhances the tissue resistance to rupture at cell-cell junctions. As cohesion is at the heart of epithelial physiology, our model may be relevant to many other epithelial systems, even if manifested at different time/length scales. SignificanceOur work demonstrates that many observed dynamical phenomena in epithelial tissues can be explained merely by mechanical cell-cell interactions, and do not require chemical diffusion or transport between cells (though chemical activity may participate in relevant intracellular processes). Specifically, we show that single cell extension-induced-contraction (EIC) is sufficient to generate propagating contraction pulses, which also increase the tissues resistance to rupture, an essential function of epithelia. Our results may shed light on how epithelial tissues function under challenging physiological conditions, e.g. in lung, gut, vasculature and other biomedical contexts. Our results may also be relevant in the study of early evolution of multicellularity and the nervous-muscular systems. Finally, the work offers guidelines for designing soft synthetic solids with improved mechanical properties.

biophysics↗

Ultra-fast cellular contractions in the epithelium of T. adhaerens and the "active cohesion" hypothesis

By definition of multi-cellularity, all animals need to keep their cells attached and intact, despite internal and external forces. Cohesion between epithelial cells provides this key feature. In order to better understand fundamental limits of this cohesion, we study the epithelium mechanics of an ultra-thin (~25 um) primitive marine animal Trichoplax adhaerens, composed essentially of two flat epithelial layers. With no known extra-cellular-matrix and no nerves or muscles, T. adhaerens was claimed the \"simplest known living animal\", yet is still capable of coordinated locomotion and behavior. Here we report the discovery of the fastest epithelial cellular contractions to date to be found in T. adhaerens dorsal epithelium (50% shrinkage of apical cell area within one second, at least an order of magnitude faster than known examples). Live imaging reveals emergent contractile patterns that are mostly sporadic single-cell events, but also include propagating contraction waves across the tissue. We show that cell contraction speed can be explained by current models of non-muscle actin-myosin bundles without load, while the tissue architecture and unique mechanical properties are softening the tissue, minimizing the load on a contracting cell. We propose a hypothesis, in which the physiological role of the contraction dynamics is to avoid tissue rupture (\"active cohesion\"), a novel concept that can be further applied to engineering of active materials.\n\nOne Sentence SummaryWe report the fastest epithelial cell contractions known to date, show they fit the kinematics arising from current cytoskeletal models, and suggest the extreme tissue dynamics is a means to actively avoid rupture.

biophysics↗