Polarity-driven three-dimensional spontaneous rotation of a cell doublet

Lu, Linjie; Guyomar, Tristan; Vagne, Quentin; Berthoz, Rémi; Torres-Sánchez, Alejandro; Lieb, Michèle; Martin-Lemaitre, Cécilie; Unen, Kobus van; Honigmann, Alf; Pertz, Olivier; Salbreux, Guillaume; Riveline, Daniel

doi:10.1101/2022.12.21.521355

Cited by 2 publications

(2 citation statements)

References 35 publications

(42 reference statements)

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“…Another system where our results may be relevant is in the context of the transition from dome to wrinkle shapes in ascidian oocytes, where a myoplasm elastic layer undergoes shape deformation due to cortical myosin contractility ( 39 ). Another example comes from confined cell doublets, which interact via their (cortical) surfaces ( 40 ). These two cortical layers form a thin elastic sheet of uniform thickness, which undergoes dynamic transition between dome, wrinkled (two and three-peak saddles), and yin-yang configurations, due to variations in myosin distribution in the actin cortices.…”

Section: Discussionmentioning

confidence: 99%

Self-assembled active actomyosin gels spontaneously curve and wrinkle similar to biological cells and tissues

Livne,

Gat,

Armon

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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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, that converts chemical energy into mechanical work. A good understanding of how contractile stresses in the cytoskeleton arise into different three-dimensional (3D) shapes and what are the shape selection rules that determine their final configurations is still lacking. To obtain insight into the relevant physical mechanisms, 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, dynamically self-organize into a family of 3D shapes, such as domes and wrinkled shapes, without the need for specific preprogramming or additional regulation. Shape deformation is driven by the spontaneous emergence of stress gradients driven by myosin and is encoded in the initial disc radius to thickness aspect ratio, which may indicate shaping scalability. Our results suggest that while the dynamical pathways may depend on the detailed interactions between the different microscopic components within the gel, the final selected shapes obey the general theory of elastic deformations of thin sheets. Altogether, our results emphasize the importance for the emergence of active stress gradients for buckling-driven shape deformations and provide insights on the mechanically induced spontaneous shape transitions in contractile active matter, revealing potential shared mechanisms with living systems across scales.

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Section: Discussionmentioning

confidence: 99%

Self-assembled active actomyosin gels spontaneously curve and wrinkle similar to biological cells and tissues

Livne,

Gat,

Armon

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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“…We used 3 cellular systems, MDCK II cell lines, mouse embryonic cells (mES cells) 37 , and pancreatic spheres 38 . Other mutant cell lines were used for MDCK: MDCK II E-cadherin-GFP/Podocalyxin-mScarlett/Halo-CAAX 39 , MDCK II ZO1/2-KO 21 and MDCK II E-cadherin KO 40 .…”

Section: Methodsmentioning

confidence: 99%

Generic rules of lumen nucleation and fusion in epithelial organoids

Lu,

Fuji,

Guyomar

et al. 2024

Preprint

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Many internal organs in the body harbor a fluid-filled lumen. The mechanisms of lumens initiation and fusion have been reported as dependent on organ-type during organogenesis. In contrast, the physics of lumen suggests that force balance between luminal pressure and cell mechanics could lead to conserved rules which may unify their self-organisation. However, this hypothesis lacks experimental evidence. Here we show that lumens share similar dynamics for three different systems (MDCK cysts, pancreatic spheres, and epiblast cysts) by using quantitative cell biology, microfabrication and theory. We report that initial cell number determines the maximum number of lumens but does not impact the steady state which is a final single lumen. In addition, lumens numbers exhibit two phases over time, a nucleation phase followed by a fusion phase. In the nucleation phase, lumens form between two cells in pancreatic and MDCK cysts whereas they form at the rosette stage between ten cells in epiblasts. In the second phase, lumens fuse by an increase in lumen volume for pancreatic spheres and MDCK cysts, whereas cell convergent directional motion leads to lumens fusion in epiblasts. We support these results by reproducing numerically lumens dynamics using a phase field model with simple rules for cell proliferation, cell adhesion and lumen growth. We finally use MDCK cysts to manipulate cell adhesion and lumen volume and we successfully reproduce the fusion dynamics of pancreatic spheres and epiblasts. Our results reveal self-organisation rules of lumens across systems with relevance for morphogenesis during development and for the design of synthetic organs.

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Polarity-driven three-dimensional spontaneous rotation of a cell doublet

Cited by 2 publications

References 35 publications

Self-assembled active actomyosin gels spontaneously curve and wrinkle similar to biological cells and tissues

Self-assembled active actomyosin gels spontaneously curve and wrinkle similar to biological cells and tissues

Generic rules of lumen nucleation and fusion in epithelial organoids

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