Large-scale mechanical properties of
            <i>Xenopus</i>
            embryonic epithelium

Luu, Olivia; David, Robert; Ninomiya, H.; Winklbauer, Rudolf

doi:10.1073/pnas.1010331108

Cited by 66 publications

(76 citation statements)

References 36 publications

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“…5B). Cells are considered to exert an elastic restoring force to maintain cell appearance (Luu et al, 2011;Nagai and Honda, 2001). Vertices were assumed to move to maintain the length of the basal edge and cell perimeter based on our morphometric results (Fig.…”

Section: Resultsmentioning

confidence: 99%

Modulation of apical constriction by Wnt signaling is required for lung epithelial shape transition

Fumoto

Takigawa-Imamura

Sumiyama³

et al. 2016

Development

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In lung development, the apically constricted columnar epithelium forms numerous buds during the pseudoglandular stage. Subsequently, these epithelial cells change shape into the flat or cuboidal pneumocytes that form the air sacs during the canalicular and saccular (canalicular-saccular) stages, yet the impact of cell shape on tissue morphogenesis remains unclear. Here, we show that the expression of Wnt components is decreased in the canalicularsaccular stages, and that genetically constitutive activation of Wnt signaling impairs air sac formation by inducing apical constriction in the epithelium as seen in the pseudoglandular stage. Organ culture models also demonstrate that Wnt signaling induces apical constriction through apical actomyosin cytoskeletal organization. Mathematical modeling reveals that apical constriction induces bud formation and that loss of apical constriction is required for the formation of an air sac-like structure. We identify MAP/microtubule affinity-regulating kinase 1 (Mark1) as a downstream molecule of Wnt signaling and show that it is required for apical cytoskeletal organization and bud formation. These results suggest that Wnt signaling is required for bud formation by inducing apical constriction during the pseudoglandular stage, whereas loss of Wnt signaling is necessary for air sac formation in the canalicular-saccular stages.

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Section: Resultsmentioning

confidence: 99%

Modulation of apical constriction by Wnt signaling is required for lung epithelial shape transition

Fumoto

Takigawa-Imamura

Sumiyama³

et al. 2016

Development

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“…Previous biomechanical analyses of gastrula stages in Xenopus embryos (Beloussov et al, 2006;Zhou et al, 2009Zhou et al, , 2010von Dassow et al, 2010von Dassow et al, , 2014Luu et al, 2011) have suggested that mechanical feedback mechanisms operate during development to allow robust morphogenetic movements. Force production in dorsal tissues is needed to deform both those tissues and the rest of the embryo.…”

Section: Discussionmentioning

confidence: 99%

Force production and mechanical accommodation during convergent extension

et al. 2015

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Forces generated within the embryo during convergent extension (CE) must overcome mechanical resistance to push the head away from the rear. As mechanical resistance increases more than eightfold during CE and can vary twofold from individual to individual, we have proposed that developmental programs must include mechanical accommodation in order to maintain robust morphogenesis. To test this idea and investigate the processes that generate forces within early embryos, we developed a novel gel-based sensor to report force production as a tissue changes shape; we find that the mean stress produced by CE is 5.0±1.6 Pascal (Pa). Experiments with the gel-based force sensor resulted in three findings.(1) Force production and mechanical resistance can be coupled through myosin contractility. The coupling of these processes can be hidden unless affected tissues are challenged by physical constraints. (2) CE is mechanically adaptive; dorsal tissues can increase force production up to threefold to overcome a stiffer microenvironment. These findings demonstrate that mechanical accommodation can ensure robust morphogenetic movements against environmental and genetic variation that might otherwise perturb development and growth. (3) Force production is distributed between neural and mesodermal tissues in the dorsal isolate, and the notochord, a central structure involved in patterning vertebrate morphogenesis, is not required for force production during late gastrulation and early neurulation. Our findings suggest that genetic factors that coordinately alter force production and mechanical resistance are common during morphogenesis, and that their cryptic roles can be revealed when tissues are challenged by controlled biophysical constraints.

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“…Tissue explants, after having rounded up under the influence of surface tension, deviate from a spherical equilibrium shape due to gravity. We used this effect to determine tissue surface tension σ (Del Rio and Neumann, 1997; David et al, 2009;Luu et al, 2011) as a measure of cohesion (Box 1, Fig. 1A, Table 1; supplementary material Fig.…”

Section: Relationship Between Tissue Surface Tension and Tissue Viscomentioning

confidence: 99%

“…1B; supplementary mathematical analyses, Section 2). Observation started about 20 min after excision, when explants had taken on ellipsoidal shapes, and elastic (von Dassow and Davidson, 2009;Luu et al, 2011) and wounding (Li et al, 2013) reactions had subsided. Rounding was associated with cell rearrangement ( Fig.…”

Section: Relationship Between Tissue Surface Tension and Tissue Viscomentioning

confidence: 99%

“…Axisymmetric drop shape analysis (ADSA) (Del Rio and Neumann, 1997) was used to determine tissue surface tensions for regions of the early gastrula, as described (Luu et al, 2011). For unknown reasons, surface tension of the ectoderm, but not of the other tissues, alternated between high and low states over the course of many months (although apparently not in a seasonal rhythm).…”

Section: Measurements Of Cell and Tissue Parametersmentioning

confidence: 99%

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Tissue cohesion and the mechanics of cell rearrangement

et al. 2014

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Morphogenetic processes often involve the rapid rearrangement of cells held together by mutual adhesion. The dynamic nature of this adhesion endows tissues with liquid-like properties, such that largescale shape changes appear as tissue flows. Generally, the resistance to flow (tissue viscosity) is expected to depend on the cohesion of a tissue (how strongly its cells adhere to each other), but the exact relationship between these parameters is not known. Here, we analyse the link between cohesion and viscosity to uncover basic mechanical principles of cell rearrangement. We show that for vertebrate and invertebrate tissues, viscosity varies in proportion to cohesion over a 200-fold range of values. We demonstrate that this proportionality is predicted by a cell-based model of tissue viscosity. To do so, we analyse cell adhesion in Xenopus embryonic tissues and determine a number of parameters, including tissue surface tension (as a measure of cohesion), cell contact fluctuation and cortical tension. In the tissues studied, the ratio of surface tension to viscosity, which has the dimension of a velocity, is 1.8 µm/min. This characteristic velocity reflects the rate of cell-cell boundary contraction during rearrangement, and sets a limit to rearrangement rates. Moreover, we propose that, in these tissues, cell movement is maximally efficient. Our approach to cell rearrangement mechanics links adhesion to the resistance of a tissue to plastic deformation, identifies the characteristic velocity of the process, and provides a basis for the comparison of tissues with mechanical properties that may vary by orders of magnitude.

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Large-scale mechanical properties of Xenopus embryonic epithelium

Cited by 66 publications

References 36 publications

Modulation of apical constriction by Wnt signaling is required for lung epithelial shape transition

Modulation of apical constriction by Wnt signaling is required for lung epithelial shape transition

Force production and mechanical accommodation during convergent extension

Tissue cohesion and the mechanics of cell rearrangement

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