Natural variation in embryo mechanics: gastrulation in <i>Xenopus laevis</i> is highly robust to variation in tissue stiffness

Dassow, Michelangelo von; Davidson, Lance A.

doi:10.1002/dvdy.21809

Cited by 52 publications

(57 citation statements)

References 64 publications

(88 reference statements)

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“…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%

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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Section: Relationship Between Tissue Surface Tension and Tissue Viscomentioning

confidence: 99%

Tissue cohesion and the mechanics of cell rearrangement

et al. 2014

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“…We still know little about either the magnitude or the sources of natural variation in embryo mechanics, but a few studies have attempted to rigorously quantify embryo-to-embryo or clutch-to-clutch variation in the mechanical properties of embryos or embryonic tissues. These studies indicate substantial variation in tissue compliance in gastrula stage frog and sea urchin embryos (von Dassow and Davidson, 2007, von Dassow and Davidson, 2009) and in the apparent surface tension in frog cell aggregates (Kalantarian et al, 2009). …”

Section: Sources Of Mechanical Variationmentioning

confidence: 87%

Physics and the canalization of morphogenesis: a grand challenge in organismal biology

Dassow

Davidson

2011

Phys. Biol.

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Morphogenesis takes place in a background of organism-to-organism and environmental variation. Therefore, a fundamental question in the study of morphogenesis is how the mechanical processes of tissue movement and deformation are affected by that variability, and in turn, how the mechanics of the system modulates phenotypic variation. We highlight a few key factors, including environmental temperature, embryo size, and environmental chemistry that might perturb the mechanics of morphogenesis in natural populations. Then we discuss several ways in which mechanics – including feedback from mechanical cues – might influence intra-specific variation in morphogenesis. To understand morphogenesis it will be necessary to consider whole-organism, environment, and evolutionary scales because these larger scales present the challenges that developmental mechanisms have evolved to cope with. Studying the variation organisms express and the variation organisms experience will aid in deciphering the causes of birth defects.

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“…It will be important to verify this type of approach in systems in which one can directly measure tissue mechanics, and Lance Davidson (University of Pittsburgh, USA) showed how classical amphibian microsurgery and explant techniques can be used to do just this and how, in the process, they made the surprising discovery that morphogenesis in Xenopus is robust to natural twofold variations in mechanical properties (von Dassow and Davidson, 2009) and to significant variation in applied forces (von Dassow et al, 2011).…”

Section: A Glimpse Of the Futurementioning

confidence: 99%

Making waves: the rise and fall and rise of quantitative developmental biology

Davidson

Baum

2012

Development

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The tenth annual RIKEN Center for Developmental Biology symposium 'Quantitative Developmental Biology' held in March 2012 covered a range of topics from coat colour patterning to the mechanics of morphogenesis. The studies presented shared a common theme in which a combination of physical theory, quantitative analysis and experiment was used to understand a specific cellular process in development. This report highlights these innovative studies and the long-standing questions in developmental biology that they seek to answer.

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Natural variation in embryo mechanics: gastrulation in Xenopus laevis is highly robust to variation in tissue stiffness

Cited by 52 publications

References 64 publications

Tissue cohesion and the mechanics of cell rearrangement

Tissue cohesion and the mechanics of cell rearrangement

Physics and the canalization of morphogenesis: a grand challenge in organismal biology

Making waves: the rise and fall and rise of quantitative developmental biology

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