3D viscoelastic drag forces contribute to cell shape changes during organogenesis in the zebrafish embryo

Sanematsu, Paula C.; Erdemci-Tandogan, Gonca; Patel, Himani; Retzlaff, Emma M.; Amack, Jeffrey D.; Manning, M. Lisa

doi:10.1016/j.cdev.2021.203718

Cited by 15 publications

(10 citation statements)

References 47 publications

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“…Interestingly, in ordered ground states of the model, there is a distinction between the onset of rigidity determined by the shear modulus (which occurs at the shape index of a regular hexagon, p 0 ∼ 3.72), and when energy barriers disappear (at ). This suggests that there must be non-analytic cusps in the potential energy landscape Sussman and Merkel (2018 ); Popović et al (2021 ) and that there may be significant differences between the linear (zero strain rate, infinitesimal strain) and nonlinear (finite strain rate, finite strain) rheology of vertex models, which have recently been studied in 2D Duclut et al (2021 ); Basan et al (2011 ); Popović et al (2021 ) and 3D Sanematsu et al (2021 ).…”

Section: Models and Methodsmentioning

confidence: 99%

Universality in the Mechanical Behavior of Vertex Models for Biological Tissues

Damavandi

Lawson-Keister

Manning

2022

Preprint

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For confluent or nearly confluent tissues, simulations and analyses of simple vertex models – where the cell shape is defined as a network of edges and vertices – have proven useful for making predictions about mechanics and collective behavior, including rigidity transitions. Scientists have developed many versions of vertex models with different assumptions. Here we investigate a set of vertex models which differ in the functional form that describes how energy depends on the vertex positions. We analyze whether such models have a well-defined shear modulus in the limit of zero applied strain rate, and if so how that modulus depends on model parameters. We identify a class of models with a well-defined shear modulus, and demonstrate that these models do exhibit a cross-over from a soft or floppy regime to a stiff regime as a function of a single control parameter, similar to the standard vertex model. Moreover, and perhaps more surprisingly, the rigidity crossover is associated with a crossover in the observed cell shape index (the ratio of the cell perimeter to the square root of the cell area), just as in the standard vertex model, even though the control parameters are different. This suggests that there may be a broad class of vertex models with these universal features, and helps to explain why vertex models are able to robustly predict these features in experiments.

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Section: Models and Methodsmentioning

confidence: 99%

Universality in the Mechanical Behavior of Vertex Models for Biological Tissues

Damavandi

Lawson-Keister

Manning

2022

Preprint

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“…Specifically, the model predicts these drag forces depend on the rate of movement of KV and fluid-like properties of the tailbud tissue. In follow up work, Sanematsu, et al (Sanematsu et al, 2021) developed a 3D model of KV moving through tailbud tissue to further characterize drag forces on KV. 3D simulations and quantitative analyses of KV movement relative to tailbud cells in live embryos indicated KV experiences drag forces that contribute to KV cell shape changes.…”

Section: Recent Findingsmentioning

confidence: 99%

Understanding laterality disorders and the left-right organizer: Insights from zebrafish

Forrest

Barricella²,

Pohar³

et al. 2022

Front. Cell Dev. Biol.

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Vital internal organs display a left-right (LR) asymmetric arrangement that is established during embryonic development. Disruption of this LR asymmetry—or laterality—can result in congenital organ malformations. Situs inversus totalis (SIT) is a complete concordant reversal of internal organs that results in a low occurrence of clinical consequences. Situs ambiguous, which gives rise to Heterotaxy syndrome (HTX), is characterized by discordant development and arrangement of organs that is associated with a wide range of birth defects. The leading cause of health problems in HTX patients is a congenital heart malformation. Mutations identified in patients with laterality disorders implicate motile cilia in establishing LR asymmetry. However, the cellular and molecular mechanisms underlying SIT and HTX are not fully understood. In several vertebrates, including mouse, frog and zebrafish, motile cilia located in a “left-right organizer” (LRO) trigger conserved signaling pathways that guide asymmetric organ development. Perturbation of LRO formation and/or function in animal models recapitulates organ malformations observed in SIT and HTX patients. This provides an opportunity to use these models to investigate the embryological origins of laterality disorders. The zebrafish embryo has emerged as an important model for investigating the earliest steps of LRO development. Here, we discuss clinical characteristics of human laterality disorders, and highlight experimental results from zebrafish that provide insights into LRO biology and advance our understanding of human laterality disorders.

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“…Although our 1D model successfully captured the inflation response dynamics of MDCK cysts under various experimental conditions, DC stimulation necessarily assigns a directionality to our system with cations and anions moving anti-parallel along the field. To fully capture the spatiotemporal ion dynamics in our system, we consider a 2D continuum model building upon previous work on electro-osmotic ion transport [66,67], motivated by the in vivo relevance of electro-osmotic flow in organ development [68]. Rather than reflect long-term mechanical changes, this 2D model was specifically created to capture the transient ionic gradient dynamics that might underlie the asymmetric responses we observe.…”

Section: Asymmetrical Morphology Of Electrically Stimulated Mdck Cystsmentioning

confidence: 99%

Pump it up: bioelectric stimulation controls tissue hydrostatic pressure and water transport via electro-inflation

Shim

Breinyn

Martínez-Calvo

et al. 2022

Preprint

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Epithelial tissues sheath many organs, separating ‘outside’ from ‘inside’ and exquisitely regulating ion and water transport via electromechanical pumping to maintain homeostatic balance and tissue hydrostatic pressure. While it is becoming increasingly clear that the ionic microenvironment and external electric stimuli can affect epithelial function and behavior, the coupling between electrical perturbation and tissue form remain unclear. We investigated this by combining electrical stimulation with three-dimensional epithelial tissues with hollow ‘lumens’—both kidney cysts and complex intestinal stem cell organoids. Our core finding is that physiological strength electrical stimulation of order 1-3 V/cm (with both direct and alternating currents) can drive powerful and rapid inflation of hollow tissues through a process we call ‘electro-inflation’, inducing a nearly threefold increase in tissue volume and striking asymmetries in tissue form. Electro-inflation is primarily driven by activation of the CFTR ion channel pumping chloride into the tissue, causing water to osmotically flow. This influx generates hydrostatic pressure, and inflation results from a competition between this pressure and cell cytoskeletal tension. We validated these interpretations with computational models connecting ion dynamics in the Diffuse Double Layer around tissues to tissue mechanics. Electro-inflation is a unique biophysical process to study and control complex tissue function.

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3D viscoelastic drag forces contribute to cell shape changes during organogenesis in the zebrafish embryo

Cited by 15 publications

References 47 publications

Universality in the Mechanical Behavior of Vertex Models for Biological Tissues

Universality in the Mechanical Behavior of Vertex Models for Biological Tissues

Understanding laterality disorders and the left-right organizer: Insights from zebrafish

Pump it up: bioelectric stimulation controls tissue hydrostatic pressure and water transport via electro-inflation

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