Epithelial organ shape is generated by patterned actomyosin contractility and maintained by the extracellular matrix

Nematbakhsh, Ali; Levis, Megan; Kumar, Nilay; Chen, Weitao; Zartman, Jeremiah J.; Alber, Mark

doi:10.1371/journal.pcbi.1008105

Cited by 34 publications

(65 citation statements)

References 58 publications

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“…3, b and e ). There is also actomyosin-mediated tension along the basal surface of wing pouch cells, which contributes to the curvature of the wing pouch ( Nematbakhsh et al 2020 ). Wing disc cells have filopodial extensions near their basal side, which can extend over a few cell diameters and have been implicated in Notch signaling ( de Joussineau et al 2003 ).…”

Section: Cell Biology Of the Wing Discmentioning

confidence: 99%

The wing imaginal disc

Tripathi

Irvine

2022

Genetics

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The Drosophila wing imaginal disc is a tissue of undifferentiated cells that are precursors of the wing and most of the notum of the adult fly. The wing disc first forms during embryogenesis from a cluster of ∼30 cells located in the second thoracic segment, which invaginate to form a sac-like structure. They undergo extensive proliferation during larval stages to form a mature larval wing disc of ∼35,000 cells. During this time, distinct cell fates are assigned to different regions, and the wing disc develops a complex morphology. Finally, during pupal stages the wing disc undergoes morphogenetic processes and then differentiates to form the adult wing and notum. While the bulk of the wing disc comprises epithelial cells, it also includes neurons and glia, and is associated with tracheal cells and muscle precursor cells. The relative simplicity and accessibility of the wing disc, combined with the wealth of genetic tools available in Drosophila, have combined to make it a premier system for identifying genes and deciphering systems that play crucial roles in animal development. Studies in wing imaginal discs have made key contributions to many areas of biology, including tissue patterning, signal transduction, growth control, regeneration, planar cell polarity, morphogenesis, and tissue mechanics.

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Section: Cell Biology Of the Wing Discmentioning

confidence: 99%

The wing imaginal disc

Tripathi

Irvine

2022

Genetics

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“…In particular, the turnover of adult BM may need to be revisited using in vivo techniques, such as FRAP. Computational models with an explicit implementation of BM have already shed light on how BM mechanics can affect tissue shape [71,138]. Better experimental characterization of changes in BM mechanics is beneficial for these models, as it will improve their parametrization and therefore predictive power.…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

To form and function: on the role of basement membrane mechanics in tissue development, homeostasis and disease

Khalilgharibi

Mao

2021

Open Biol.

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The basement membrane (BM) is a special type of extracellular matrix that lines the basal side of epithelial and endothelial tissues. Functionally, the BM is important for providing physical and biochemical cues to the overlying cells, sculpting the tissue into its correct size and shape. In this review, we focus on recent studies that have unveiled the complex mechanical properties of the BM. We discuss how these properties can change during development, homeostasis and disease via different molecular mechanisms, and the subsequent impact on tissue form and function in a variety of organisms. We also explore how better characterization of BM mechanics can contribute to disease diagnosis and treatment, as well as development of better in silico and in vitro models that not only impact the fields of tissue engineering and regenerative medicine, but can also reduce the use of animals in research.

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“…The model was implemented in the framework of subcellular element method (SEM) [34] which represents a cell by a collection of elements (particles in 3D space). The spatial dynamics of the cells depicted by these elements partially depend on the modeled gene expression and, in turn, provide a spatial reference for modeling intercellular gene regulations [7,35,36]. The following aspects are accounted for: cell-cell interactions; selective adhesion; cell division; confinement of cells by the zona pellucida; and cavity formation (see Eq (7) and S1 Text section 1 for details).…”

Section: A Multiscale Three-dimensional Model From Fertilization (1 Cmentioning

confidence: 99%

A multiscale model via single-cell transcriptomics reveals robust patterning mechanisms during early mammalian embryo development

Cang

Wang

et al. 2021

PLoS Comput Biol

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During early mammalian embryo development, a small number of cells make robust fate decisions at particular spatial locations in a tight time window to form inner cell mass (ICM), and later epiblast (Epi) and primitive endoderm (PE). While recent single-cell transcriptomics data allows scrutinization of heterogeneity of individual cells, consistent spatial and temporal mechanisms the early embryo utilize to robustly form the Epi/PE layers from ICM remain elusive. Here we build a multiscale three-dimensional model for mammalian embryo to recapitulate the observed patterning process from zygote to late blastocyst. By integrating the spatiotemporal information reconstructed from multiple single-cell transcriptomic datasets, the data-informed modeling analysis suggests two major processes critical to the formation of Epi/PE layers: a selective cell-cell adhesion mechanism (via EphA4/EphrinB2) for fate-location coordination and a temporal attenuation mechanism of cell signaling (via Fgf). Spatial imaging data and distinct subsets of single-cell gene expression data are then used to validate the predictions. Together, our study provides a multiscale framework that incorporates single-cell gene expression datasets to analyze gene regulations, cell-cell communications, and physical interactions among cells in complex geometries at single-cell resolution, with direct application to late-stage development of embryogenesis.

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Epithelial organ shape is generated by patterned actomyosin contractility and maintained by the extracellular matrix

Cited by 34 publications

References 58 publications

The wing imaginal disc

The wing imaginal disc

To form and function: on the role of basement membrane mechanics in tissue development, homeostasis and disease

A multiscale model via single-cell transcriptomics reveals robust patterning mechanisms during early mammalian embryo development

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