Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation

Fierling, Julien; John, Alphy; Delorme, Barthélémy; Torzynski, Alexandre; Blanchard, Guy B.; Lye, Claire M.; Malandain, Grégoire; Sanson, Bénédicte; Etienne, Jocelyn; Marmottant, Philippe; Quilliet, Catherine; Rauzi, Matteo

doi:10.1101/2021.12.14.472566

Cited by 6 publications

(8 citation statements)

References 59 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Internal cell strain, which is likely significant during cellular process such as cell division[38], can also be considered as a source of external loading. Finally, transient and reversible AB-T1 transitions have been observed [39, 40]; the dynamic aspect of AB-T1 transitions may be relevant to the mechanism of T1 transitions [23, 36] and their contributions to processes like tissue folding or buckling [41−46] remains to be investigated.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Curvature-induced cell rearrangements in biological tissues

Lou

Rupprecht

Hiraiwa

et al. 2022

Preprint

View full text Add to dashboard Cite

On a curved surface, epithelial cells can adapt to geometric constraints by tilting and by exchanging their neighbors from apical to basal sides, known as an apicobasal T1 (AB-T1) transition. The relationship between cell tilt, AB-T1 transitions, and tissue curvature still lacks a unified understanding. Here, we propose a general framework for cell packing in curved environments and explain the formation of AB-T1 transitions under different conditions. We find that steep curvature gradients can lead to cell tilting and induce AB-T1 transitions. Conversely, large curvature anisotropy can drive AB-T1 transitions by hydrostatic pressure. The two mechanisms compete to determine the impact of tissue geometry and mechanics on optimized cell rearrangements in 3D.

show abstract

Section: Discussionmentioning

confidence: 99%

“…Finally, transient and reversible AB-T1 transitions have 304 been observed [39,40]; the dynamic aspect of AB-T1 305 transitions may be relevant to the mechanism of T1 tran-306 sitions [23,36] and their contributions to processes like 307 tissue folding or buckling [41][42][43][44][45][46] remains to be investi-308 gated.…”

mentioning

confidence: 99%

Curvature-induced cell rearrangements in biological tissues

Lou

Rupprecht

Hiraiwa

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…As mentioned in §2.2, the dynamics of the system can come either from an evolution of the prestress or from a passive relaxation of the material. With some notable exceptions [94], the evolution of the prestress is generally slower than the relaxation of the material. Indeed, biopolymer networks are in general very dynamic as they are being constantly remodelled by processes of (de)reticulation and (de)polymerization.…”

Section: Prestress In Biopolymer Networkmentioning

confidence: 99%

“…Recent data from the ventral furrow formation in Drosophila embryos showed the importance of the global ellipsoidal geometry of the embryo for an elongated ventral patch of myosin to achieve a fold along its long axis [131]. Indeed, heterogeneous prestress at the surface of a thin shell respecting this geometry leads to surface buckling initiating folding with the correct pattern of strain and dynamics [94].…”

Section: Prestress In Cellularized Tissuementioning

confidence: 99%

How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale

et al. 2022

Self Cite

View full text Add to dashboard Cite

Cells and tissues change shape both to carry out their function and during pathology. In most cases, these deformations are driven from within the systems themselves. This is permitted by a range of molecular actors, such as active crosslinkers and ion pumps, whose activity is biologically controlled in space and time. The resulting stresses are propagated within complex and dynamical architectures like networks or cell aggregates. From a mechanical point of view, these effects can be seen as the generation of prestress or prestrain, resulting from either a contractile or growth activity. In this review, we present this concept of prestress and the theoretical tools available to conceptualize the statics and dynamics of living systems. We then describe a range of phenomena where prestress controls shape changes in biopolymer networks (especially the actomyosin cytoskeleton and fibrous tissues) and cellularized tissues. Despite the diversity of scale and organization, we demonstrate that these phenomena stem from a limited number of spatial distributions of prestress, which can be categorized as heterogeneous, anisotropic or differential. We suggest that in addition to growth and contraction, a third type of prestress—topological prestress—can result from active processes altering the microstructure of tissue.

show abstract

“…So far, numerous studies have explored how mechanical force production and tissue mechanical properties control the dynamics of tissue invaginations 7,8 . These studies have defined several mechanisms associated with fold formation including: (i) cell apical constriction for which the surface area or anisotropy of the constricting domain could modulate fold shape [9][10][11][12][13][14][15][16][17][18] ; (ii) apical-basal shortening of the cells [19][20][21][22] ; (iii) cell delamination 23,24 ; and (iv) tissue buckling due to compressive stresses 11,[25][26][27][28][29][30][31] . Despite these advances, whether and how epithelial folding dynamics is regulated by curvature, an intrinsic property of any epithelia, has remained unexplored during development.…”

Section: Introductionmentioning

confidence: 99%

Homeotic compartment curvature and tension control spatiotemporal folding dynamics

Villedieu

Alpar

Gaugué

et al. 2022

Preprint

View full text Add to dashboard Cite

Shape is a conspicuous and fundamental property of biological systems entailing the function of organs and tissues. While much emphasis has been put on how tissue tension and mechanical properties drive shape changes, whether and how a given tissue geometry influences subsequent morphogenesis remains poorly characterized. Here, we explored how curvature, a key descriptor of tissue geometry, impinges on the dynamics of epithelial tissue invagination. We found that the morphogenesis of the fold separating the adult Drosophila head and thorax segments is driven by the invagination of the Deformed (Dfd) homeotic compartment. Dfd controls invagination by modulating actomyosin organization and in-plane epithelial tension via the Tollo and Dystroglycan receptors. By experimentally introducing curvature heterogeneity within the homeotic compartment, we established that a curved tissue geometry converts the Dfd-dependent in-plane tension into an inward force driving folding. Accordingly, the interplay between in-plane tension and tissue curvature quantitatively explains the spatiotemporal folding dynamics. Collectively, our work highlights how genetic patterning and tissue geometry provide a simple design principle driving folding morphogenesis during development.

show abstract

Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation

Cited by 6 publications

References 59 publications

Curvature-induced cell rearrangements in biological tissues

Curvature-induced cell rearrangements in biological tissues

How dynamic prestress governs the shape of living systems, from the subcellular to tissue scale

Homeotic compartment curvature and tension control spatiotemporal folding dynamics

Contact Info

Product

Resources

About