Active nematics across scales from cytoskeleton organization to tissue morphogenesis

Balasubramaniam, Lakshmi; Mège, René-Marc; Ladoux, Benoît

doi:10.1016/j.gde.2021.101897

Cited by 29 publications

(22 citation statements)

References 79 publications

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“…As in molecular liquid crystals, orientational order can be locally disrupted by topological defects, point-like singularities where the cells' local orientation is undefined. In multicellular systems, topological defects are believed to serve various kind of biological functionalities, from driving collective motion at length scales significantly larger than that of individual cells 14,24 , to facilitate the extrusion of apoptotic cells 15 , and the development of sharp features, such as tentacles and protrusions 26,38 .…”

Section: Multiscale Hexanematic Order Strengthen With the Monolayer D...mentioning

confidence: 99%

“…Among the various aspect of multicellular organization, orientational order has recently been identified as an essential concept, because of its inherent propensity towards enhancing the coherence of microscopic forces that would be incoherent (randomly oriented) otherwise [13][14][15][16][17][18][19] . Elongated cells, such as fibroblasts 13 , neurons 14 , and potentially any mesenchymal phenotypes, tend, for instance, to align with each other, thereby giving rise to polar 20,21 or nematic 14,15,[22][23][24] phases, whose spatial structure and dynamics facilitate a number of biomechanical processes. These include the onset of organism-wide cellular flows during gastrulation 25 , the development of protrusion and tentacles-like features 18,26 , or the extrusion of apoptotic cells 15 .…”

Section: Introductionmentioning

confidence: 99%

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Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density

Eckert

Ladoux

Giomi

et al. 2022

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During tissue folding in developmental processes and monolayer migration in wound healing, epithelial cells undergo shape changes and move collectively. Recent experimental and numerical results suggested that these processes could leverage on the existence of both nematic (2--fold) and hexatic (6--fold) orientational order coexisting at different length scales within the same epithelial layer. Yet, how this remarkable example of multiscale organization in living matter is affected by the material properties of the cells and their substrate is presently unknown. In the current article, we experimentally address these questions in monolayers of Madin-Darby canine kidney cells (MDCK-II) having various cell density and molecular repertoire. At small length scales, confluent monolayers are characterized by a prominent hexatic order and nearly vanishing nematic order, independently on the presence of E-cadherin, the monolayer density, and the underlying substrate stiffness. All three properties, however, dramatically affect the organization of MDCK-II monolayers at large length scales, where nematic order becomes dominant over hexatic order. In particular, we find that the length scale at which nematic order prevails over hexatic order -- here referred to as hexanematic crossover scale -- strongly depends on cell-cell adhesions and correlates with the monolayer density. Our analysis sheds light on how the organization of epithelial layers is affected by the material and mechanical properties, and provides a robust approach for analyzing the tissue composition towards understanding developmental processes.

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Section: Multiscale Hexanematic Order Strengthen With the Monolayer D...mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density

Eckert

Ladoux

Giomi

et al. 2022

Preprint

Self Cite

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“…For instance, in biology, the cell membrane is the key confining entity for intracellular selforganisation, but at the same time it defines the cell as an individual unit for multicellular organisation of tissues and organs, thus enabling complex functionalities to emerge. Importantly, the shape and chemical composition of the cell membrane is continuously evolving due to both mechanical and chemical stimuli from the surrounding tissue [50] and from the cell's interior, thus acting as a mediator of the feedback between different scales. The overarching key challenge here is to elucidate, measure and model how (and when) confinement at different scales mediates or separates the cross-talk and interdependence between scales.…”

Section: Overarching Scientific Challengesmentioning

confidence: 99%

Steering self-organisation through confinement

Araújo¹,

Janssen²,

Barois³

et al. 2022

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Self-organisation is the spontaneous emergence of spatio-temporal structures and patterns from the interaction of smaller individual units. Examples are found across many scales in very different systems and scientific disciplines, from physics, materials science and robotics to biology, geophysics and astronomy. Recent research has highlighted how self-organisation can be both mediated and controlled by confinement. Confinement occurs through interactions with boundaries, and can function as either a catalyst or inhibitor of self-organisation. It can then become a means to actively steer the emergence or suppression of collective phenomena in space and time. Here, to provide a common framework for future research, we examine the role of confinement in self-organisation and identify overarching scientific challenges across disciplines that need to be addressed to harness its full scientific and technological potential. This framework will not only accelerate the generation of a common deeper understanding of selforganisation but also trigger the development of innovative strategies to steer it through confinement, with impact, e.g., on the design of smarter materials, tissue engineering for biomedicine and crowd management.

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“…Reconstituted mixtures of actin or microtubule filaments with motor proteins self-organize into moving swarms, vortices, and travelling waves 1,5,8 . In living systems, such emergent behaviors can underlie a wealth of key biological phenomena such as single and collective cell motility 9,10 , cell division 11 and organism morphogenesis 12,13 .…”

Section: Introductionmentioning

confidence: 99%

Chiral and nematic phases of flexible active filaments

Dunajova

Mateu

Radler

et al. 2022

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The emergence of large-scale order in self-organized systems relies on local interactions between individual components. During bacterial cell division, the tubulin-homolog FtsZ polymerizes into treadmilling filaments that further assemble into a cytoskeletal ring. Although minimal in vitro assays have shown the striking self-organization capacity of FtsZ filaments, such as dynamic chiral assemblies, how these large-scale structures emerge and relate to individual filament properties remains poorly understood. To understand this quantitatively, we combined minimal chiral active matter simulations with biochemical reconstitution experiments. Using STED and TIRF microscopy as well as high-speed AFM, we imaged the behavior of FtsZ filaments on different spatial scales. Simulations and experiments revealed that filament density and flexibility define the local and global order of the system: At intermediate densities, flexible filaments organize into chiral rings and polar bands, while an effectively nematic organization dominates for high filament densities and for mutant filaments with increased rigidity. Our predicted phase diagram captured these features quantitatively, demonstrating how filament flexibility, density and chirality cooperate with activity to give rise to a large repertoire of collective behaviors. These properties are likely important for the dynamic organization of soft chiral matter, including that of treadmilling FtsZ filaments during bacterial cell division.

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Active nematics across scales from cytoskeleton organization to tissue morphogenesis

Cited by 29 publications

References 79 publications

Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density

Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density

Steering self-organisation through confinement

Chiral and nematic phases of flexible active filaments

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