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

Armon, Shahaf; Bull, Matthew S.; Moriel, Avraham; Aharoni, Hillel; Prakash, Manu

doi:10.1101/2020.06.15.153163

Cited by 4 publications

(8 citation statements)

References 37 publications

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“…By studying the response as a function of different size external stimuli, we reveal a threshold-like function above which the cilia is able to take a step and below which it remains on the surface and relaxes back toward the stalled position with an exponential relaxation. This re-sponse pattern is reminiscent to other nonlinear dynamical systems which are far from equilibrium such as the FitzHugh-Nagumo equation [57] except that this dynamical response is chemomechanical more similar in flavor to mechano-chemical excitability observed in the actomyosin cortex [13,15].…”

Section: Walking Cilia Are Sensitive To External Stimulimentioning

confidence: 53%

“…The organism has a top-bottom symmetry breaking [39]. The top tissue is characterized by fast cellular contractions [40] which are thought to aid in tissue cohesion [13]. The bottom tissue is made up mixture of mechanically distinct cells [41] each with their own cilium [42].…”

Section: Model Organismmentioning

confidence: 99%

“…There is still much work to be done understanding how ciliary mechanical excitability interacts with the upper epithelium's cortical excitability [13] and a more deep relationship to small signaling molecules [44,46,56]. We look forward to the lessons this 'simple' animal can teach us in how these systems can be wired together.…”

Section: Excitable Mechanics Complement Chemical Excitabilitymentioning

confidence: 99%

“…One of the recurring themes within these compliant physical reservoirs [11] of sufficiently nonlinear dynamics, is the emergence of the dynamical motif of excitability. Excitability and its related cousin -bi-stability -with a slow recovery variable is best known in the Hodgkin-Huxley equation for neurons but manifests itself much more broadly from cortical excitability [12][13][14][15], bio-electricity [16], non-neuronal excitability [17], and hydrodynamically mediated trigger waves [18].…”

Section: Introductionmentioning

confidence: 99%

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Excitable mechanics embodied in a walking cilium

Bull¹,

Kroo²,

Prakash³

2021

Preprint

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Rapid transduction of sensory stimulation to action is essential for an animal to survive. To this end, most animals use the sub-second excitable and multistable dynamics of a neuromuscular system. Here, studying an animal without neurons or muscles, we report analogous excitable and multistable dynamics embedded in the physics of a 'walking' cilium. We define a 'walking cilium' as a phenomena where the locomotive force is generated through contact with a substrate which is periodically reset by steps in the direction of motion. We begin by showing that cilia can walk without specialized gait control and identify the characteristic scales of spatiotemporal height fluctuations of the tissue. With the addition of surface interaction, we construct a low-order dynamical model of this single-cilium sub-unit. In addition to studying the dynamics of a single cilium in isolation, we subsequently examine collections of these walking cilia. En route to an emergent model for ciliary walking, we demonstrate the limits of substrate mediated synchronization between cilia. In the desynchronized limit, our model shows evidence of localized multi-stability mediated by the crosstalk between locomotive forcing and height. The out-of-equilibrium mechanics -which govern this emergent excitable bistability -directly control the locomotive forcing of a walking cilia. This direct coupling bypasses the role of the synaptic junctions between neurons and muscles. We show a minimal mechanism -trigger waves -by which these walking cells may work together to achieve organism-scale collaboration, such as coordination of hunting strikes across 10 5 cells without central control.Significance: Eukaryotic cilia are both sensors and actuators. There is a growing field of research dedicated to understanding how stimulus is transformed into action through biochemical queues within these intricate sub-cellular structures. Here, we complement this ongoing research program by considering the hypothesis that these biochemical dynamics could be outsourced to the fast timescale response of the mechanics of an oscillating cilium. To accomplish this we studied how an emerging model organism with no muscles or neurons in the phylum placozoa (plate animals) move around using ciliary "walking". To our surprise, we found that ciliary walking can be effectively described as an excitable dynamical system. We expect that these results will enrich the discussion of how cilia can be used to coordinate the behavior of many cells without a governing neuromuscular system.

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Section: Walking Cilia Are Sensitive To External Stimulimentioning

confidence: 53%

Section: Model Organismmentioning

confidence: 99%

Section: Excitable Mechanics Complement Chemical Excitabilitymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Excitable mechanics embodied in a walking cilium

Bull¹,

Kroo²,

Prakash³

2021

Preprint

Self Cite

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“…One common and simple form of communication is mediated through traveling waves [22,30,31]. Traveling waves can come in many forms from nonlinear trigger waves [32][33][34] to emergent mechanics [25,35,36], and play a fundamental role in coordinating the behavior of a collective at an incredible speed. There is a rich history coupling active mechanical work with elastic materials.…”

Section: A Agility and Information Transfer In Active Mattermentioning

confidence: 99%

Ciliary flocking and emergent instabilities enable collective agility in a non-neuromuscular animal

Bull,

Prakash,

Prakash

2021

Preprint

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Effective organismal behavior is characterized by the ability to respond appropriately to changes in the surrounding environment. Attaining this delicate balance of sensitivity and stability is a hallmark of the animal kingdom. By studying the locomotory behavior of a simple animal (Trichoplax adhaerens) without muscles or neurons, here we demonstrate how monociliated epithelial cells work collectively to give rise to an agile non-neuromuscular organism. Via direct visualization of large ciliary arrays, we report the discovery of sub-second ciliary reorientations under a rotational torque that is mediated by collective tissue mechanics and the adhesion of cilia to the underlying substrate.In an illuminating toy model, we show a mapping of this system onto an "active-elastic resonator". This framework explains how perturbations propagate information in this array as linear speed traveling waves in response to mechanical stimulus. Next, we explore the implications of periodic and noisy parametric driving in this active-elastic resonator and show that such driving can excite mechanical 'spikes'. These spikes in collective mode amplitudes are consistent with a system driven by parametric amplification and a saturating nonlinearity. We conduct extensive numerical experiments to corroborate these findings within a polarized active-elastic sheet. These results indicate that periodic and stochastic forcing are critical for increasing the sensitivity of collective ciliary flocking. We support these theoretical predictions via direct experimental observation of linear speed traveling waves which are made possible through the hybridization of spin and overdamped density waves. We map how these ciliary flocking dynamics result in agile motility via coupling between an amplified resonator and a tuning (Goldstone-like) mode of the system. This sets the stage for how activity and elasticity can self-organize into behavior which benefits the organism as a whole.

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Motility-induced fracture reveals a ductile-to-brittle crossover in a simple animal’s epithelia

Prakash

Bull

2021

Nat. Phys.

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Animals are characterized by their movement, and their tissues are continuously subjected to dynamic force loading while they crawl, walk, run or swim 1 . Tissue mechanics fundamentally determine the ecological niches that can be endured by a living organism 2 . While epithelial tissues provide an important barrier function in animals, they are subjected to extreme strains during day to day physiological activities, such as breathing 1 , feeding 3 , and defense response 4 . However, failure or inability to withstand to these extreme strains can result in epithelial fractures 5, 6 and associated diseases 7, 8 . From a materials science perspective, how properties of living cells and their interactions prescribe larger scale tissue rheology and adaptive response in dynamic force landscapes remains an important frontier 9 . Motivated by pushing tissues to the limits of their integrity, we carry out a multi-modal study of a simple yet highly dynamic organism, the Trichoplax Adhaerens 10-12 , across four orders of magnitude in length (1 µm to 10 mm), and six orders in time (0.1 sec to 10 hours). We report the discovery of abrupt, bulk epithelial tissue fractures (∼10 sec) induced by the organism's own motility. Coupled with rapid healing (∼10 min), this discovery accounts for dramatic shape change and physiological asexual division in this early-divergent metazoan. We generalize our understanding of this phenomena by codifying it in a heuristic model, highlighting the fundamental questions underlying the debonding/bonding criterion in a soft-active-living material by evoking the concept of an 'epithelial alloy'. Using a suite of quantitative experimental and numerical techniques, we demonstrate a force-driven ductile to brittle material transition governing the morphodynamics of tissues pushed to the edge of rupture. This work contributes to an important discussion at the core of developmental biology [13][14][15][16][17] , with important applications to an emerging paradigm in materials and tissue engineering 5, 18-20 , wound healing and medicine 8, 21, 22 . Tissues are the paragon example of a 'smart material'. Cells within a tissue may dynamically reconfigure under stress 15,23 , exhibit superelastic responses by localizing strain 19 , contract to actively avoid rupture 10 , locally reinforce regions of tissue through recruitment 24 and other forms of mechanically regulated feedback 25,26 . Harnessing these properties promises valuable insights for synthetic adaptable materials 18,20,27 . Many of these phenomena illustrate the role of mechanical feedback in service of tissues maintaining their integrity under large strains. Here, we address the question -how do cellular tissues behave on the threshold of failure? What determines if a tissue fractures or if it flows? We investigate this .

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

Abstract: Epithelial tissues in many contexts can be viewed as soft active solids. Their active nature is manifested

Cited by 4 publications

References 37 publications

Excitable mechanics embodied in a walking cilium

Excitable mechanics embodied in a walking cilium

Ciliary flocking and emergent instabilities enable collective agility in a non-neuromuscular animal

Motility-induced fracture reveals a ductile-to-brittle crossover in a simple animal’s epithelia

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