Epithelia are multiscale active liquid crystals

Armengol-Collado, Josep-Maria; Carenza, Livio Nicola; Eckert, Julia; Krommydas, Dimitrios; Giomi, Luca

doi:10.1038/s41567-023-02179-0

Cited by 23 publications

(11 citation statements)

References 39 publications

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“…In the more realistic case of an irregular polygon, on the other hand,

is given by the phase of the complex function

, arising form the p -fold generalization of the classic shape tensor ( Aubouy et al, 2003 ). This function was introduced in Armengol-Collado et al, 2023 and is reviewed in Methods for sake of completeness.…”

Section: Resultsmentioning

confidence: 99%

“… ( a ) Example of multiscale hexanematic order in an in vitro layer of Madin–Darby canine kidney (MDCK) cells ( b ) and its computer-constructed segmentation. Both panels are adapted from Figure 3 of Armengol-Collado et al, 2023 . The six-legged stars in the shaded region denote the sixfold orientation of the cells obtained using the approach summarized in Methods.…”

Section: Introductionmentioning

confidence: 99%

“…Shortly after discovery, the same property has been recovered within the framework of the cellular Potts model, thereby strengthening the idea that hexatic order may in fact serve as a guiding principle to unravel the collective dynamics of confluent epithelia ( Durand and Heu, 2019 ). Furthermore, recent in vitro studies of Madin–Darby canine kidney (MDCK) cell layers demonstrated that epithelial layers can in fact feature both nematic and hexatic orders, with the former being dominant at large and the latter at short length scales (see Figure 1a, b and Armengol-Collado et al, 2023 ; Eckert et al, 2023 ). This remarkable example of physical organization in biological matter, referred to as multiscale hexanematic order in Armengol-Collado et al, 2023 , is believed to complement the complex network or regulatory pathways available to individual cells to achieve multicellular organization and select specific scale-dependent collective migration strategies.…”

Section: Introductionmentioning

confidence: 99%

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Hydrodynamics and multiscale order in confluent epithelia

Armengol-Collado,

Carenza,

Giomi

2024

eLife

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We formulate a hydrodynamic theory of confluent epithelia: i.e. monolayers of epithelial cells adhering to each other without gaps. Taking advantage of recent progresses toward establishing a general hydrodynamic theory of p-atic liquid crystals, we demonstrate that collectively migrating epithelia feature both nematic (i.e. p = 2) and hexatic (i.e. p = 6) order, with the former being dominant at large and the latter at small length scales. Such a remarkable multiscale liquid crystal order leaves a distinct signature in the system's structure factor, which exhibits two different power law scaling regimes, reflecting both the hexagonal geometry of small cells clusters, as well as the uniaxial structure of the global cellular flow. We support these analytical predictions with two different cell-resolved models of epithelia - i.e. the self-propelled Voronoi model and the multiphase field model - and highlight how momentum dissipation and noise influence the range of fluctuations at small length scales, thereby affecting the degree of cooperativity between cells. Our construction provides a theoretical framework to conceptualize the recent observation of multiscale order in layers of Madin-Darby canine kidney cells and pave the way for further theoretical developments.

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“…In the more realistic case of an irregular polygon, on the other hand,

is given by the phase of the complex function

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Hydrodynamics and multiscale order in confluent epithelia

Armengol-Collado,

Carenza,

Giomi

2024

eLife

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“…S2 a). It has recently been shown in experiments and numerical simulations that cell monolayers have nematic order at large length-scales and hexatic order at small length-scales 43 , 44 and it would be of interest in future work to explore any effect of any hexatic ordering.…”

Section: Methodsmentioning

confidence: 99%

Stress-shape misalignment in confluent cell layers

Nejad,

Ruske,

McCord

et al. 2024

Nat Commun

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In tissue formation and repair, the epithelium undergoes complex patterns of motion driven by the active forces produced by each cell. Although the principles governing how the forces evolve in time are not yet clear, it is often assumed that the contractile stresses within the cell layer align with the axis defined by the body of each cell. Here, we simultaneously measured the orientations of the cell shape and the cell-generated contractile stresses, observing correlated, dynamic domains in which the stresses were systematically misaligned with the cell body. We developed a continuum model that decouples the orientations of contractile stress and cell body. The model recovered the spatial and temporal dynamics of the regions of misalignment in the experiments. These findings reveal that the cell controls its contractile forces independently from its shape, suggesting that the physical rules relating cell forces and cell shape are more flexible than previously thought.

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“…Janus particles 5–7 ) or biological origin. In this latter case, cytoskeletal suspensions 8 and cellular cultures 9–12 are examples of in vitro systems which are often employed to study active behaviors in a controlled environment, but more complex living organisms, such as developing embryos or living tissues 13–15 have recently been considered for their promising implications in understanding a variety of different biological phenomena from morphogenesis to cancer progression and spreading of infections in living organisms. Regardless of their particular realization, active systems can exploit energy to interact with the surrounding environment and perform autonomous motion, leading to a plethora of collective behaviors.…”

Section: Introductionmentioning

confidence: 99%