Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion

Li, Xinzhi; Das, Amit; Bi, Dapeng

doi:10.1103/physrevlett.123.058101

Cited by 49 publications

(79 citation statements)

References 84 publications

(92 reference statements)

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“…Second, at the regional level, the adult esophagus shows a transition towards a solid-like state in the form of heterogeneous cell patches ( Fig. 4g ); a segregation proposed to result from changes in the mechanical properties of epithelial cells 76 . This data agrees with previous work, supporting the notion that jamming transitions coordinate tissue morphogenesis by coupling the global mechanical properties of the tissue with local events at the cellular scale 41, 73 .…”

Section: Resultsmentioning

confidence: 99%

A biomechanical switch regulates the transition towards homeostasis in esophageal epithelium

McGinn

Hallou

Han

et al. 2021

Preprint

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Epithelial cells are highly dynamic and can rapidly adapt their behavior in response to tissue perturbations and increasing tissue demands. However, the processes that finely control these responses and, particularly, the mechanisms that ensure the correct switch to and from normal tissue homeostasis are largely unknown. Here we explore changes in cell behavior happening at the interface between postnatal development and homeostasis in the epithelium of the mouse esophagus, as a physiological model exemplifying a rapid but controlled tissue growth transition. Single cell RNA sequencing and histological analysis of the mouse esophagus reveal significant mechanical changes in the epithelium upon tissue maturation. Organ stretching experiments further indicate that tissue strain caused by the differential growth of the mouse esophagus relative to the entire body promotes the emergence of a defined committed population in the progenitor compartment as homeostasis is established. Our results point to a simple mechanism whereby the mechanical changes experienced at the whole tissue level are integrated with those 'sensed' at the cellular level to control epithelial cell behavior and tissue maintenance.

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Section: Resultsmentioning

confidence: 99%

A biomechanical switch regulates the transition towards homeostasis in esophageal epithelium

McGinn

Hallou

Han

et al. 2021

Preprint

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“…The unique geometry of the two-state micropattern allows a natural definition of variability in terms of the variances of the transition behaviour, which can be compared to a reference theory for this system. Our quantitative framework may help our understanding of cell-to-cell variability in collective systems [21][22][23][24]64,74] and provide useful tools for inverse approaches that attempt to correlate heterogeneity in behaviour to differences in the proteomes of single cells [64,[75][76][77][78].…”

Section: Discussionmentioning

confidence: 99%

“…phenotypic or population heterogeneity, at the level of whole-cell behaviours, such as growth rate, drug response, morphology, and migration [16][17][18][19][20]. In the case of migrating cells, CCV has profound implications at larger scales for the behaviour of cell clusters, such as their ability to chemotax [21], invade surrounding tissue [22] and perform collective motion [23,24]. Thus, CCV is increasingly well understood at the molecular level, and its implications for collective behaviour are becoming clearer.…”

Section: Introductionmentioning

confidence: 99%

Disentangling the behavioural variability of confined cell migration

Brückner

Fink

Rädler

et al. 2020

J. R. Soc. Interface.

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Cell-to-cell variability is inherent to numerous biological processes, including cell migration. Quantifying and characterizing the variability of migrating cells is challenging, as it requires monitoring many cells for long time windows under identical conditions. Here, we observe the migration of single human breast cancer cells (MDA-MB-231) in confining two-state micropatterns. To describe the stochastic dynamics of this confined migration, we employ a dynamical systems approach. We identify statistics to measure the behavioural variance of the migration, which significantly exceeds that predicted by a population-averaged stochastic model. This additional variance can be explained by the combination of an ‘ageing’ process and population heterogeneity. To quantify population heterogeneity, we decompose the cells into subpopulations of slow and fast cells, revealing the presence of distinct classes of dynamical systems describing the migration, ranging from bistable to limit cycle behaviour. Our findings highlight the breadth of migration behaviours present in cell populations.

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“…Individual cell mechanical heterogeneity can have a strong influence on the collective tissue mechanics 41 . In order to better understand these cellular scale fractures, it is useful to pinpoint the architectural differences between the two major cell types composing ventral tissue: ventral epithelial cells (size ∼ 3 µm ) and the larger lipophilic cells (size ∼ 5 µm , and comprising 13% of the ventral tissue 42 ).…”

Section: Figurementioning

confidence: 99%

“…Among the existing models to study tissue mechanics, cell-resolved tissue models have become a powerful tool for understanding rigidity transitions 41, 46, 47 , active tension networks 24 , the importance of apical-basal symmetry breaking at the cellular level 48 , how embryos generate shape 36 , and the interplay of fluidity and healing of ablated wounds 49 . Broadly, the majority of existing models have been developed to study tissue response to slow forcing timescales in confluent mono-layers with a single cell type.…”

Section: Figurementioning

confidence: 99%

Motility induced fracture reveals a ductile to brittle crossover in the epithelial tissues of a simple animal

Prakash

Bull

2019

Preprint

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8Animals 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 13-17 , with important applications to an emerging paradigm in materials and tissue engineering 5, 18-20 , wound healing and medicine 8, 21, 22 . 9 Tissues are the paragon example of a 'smart material'. Cells within a tissue may dynamically 10 reconfigure under stress 15, 23 , exhibit superelastic responses by localizing strain 19 , contract to actively 11 avoid rupture 10 , locally reinforce regions of tissue through recruitment 24 and other forms of mechanically 12 regulated feedback 25, 26 . Harnessing these properties promises valuable insights for synthetic adaptable 13 materials 18, 20, 27 . Many of these phenomena illustrate the role of mechanical feedback in service of tissues 14 maintaining their integrity under large strains. Here, we address the question -how do cellular tissues 15 behave on the threshold of failure? What determines if a tissue fractures or if it flows? We investigate this 16 question in a 'minimal tissue system' that is capable of highly adaptive and fast plastic deformation. 17 We experimentally study the dynamic epithelial tissues in the marine animal, the Trichoplax adhaerens. 1...

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Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion

Cited by 49 publications

References 84 publications

A biomechanical switch regulates the transition towards homeostasis in esophageal epithelium

A biomechanical switch regulates the transition towards homeostasis in esophageal epithelium

Disentangling the behavioural variability of confined cell migration

Motility induced fracture reveals a ductile to brittle crossover in the epithelial tissues of a simple animal

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