Tension, contraction and tissue morphogenesis

Heer, Natalie C.; Martin, Adam C.

doi:10.1242/dev.151282

Cited by 177 publications

(158 citation statements)

References 131 publications

Supporting

Mentioning

154

Contrasting

Order By: Relevance

“…Whereas the MFM incorporates part of the Hippo pathway, a description of growth also requires the integration of extrinsic growth controls, transduced via the dTOR pathway (Vollmer et al, ). The disk also is mechanically connected to the notum, the basement membrane (Domínguez‐Giménez et al, ; Pastor‐Pareja & Xu, ), apical extracellular matrix (Heer & Martin, ), peripodial cells which are opposed to the disk cells (Baena‐López et al, ), and muscles within the larva (Nienhaus et al, ). As described earlier, recent studies have shown that the basement membrane and the extracellular matrix have significant effects on the overall mechanical properties of the disk (Atzeni et al, ; Keller et al, ).…”

Section: A Model For the Control Of Disk Sizementioning

confidence: 99%

Growth control in the Drosophila wing disk

Gou

Stotsky

Othmer

2020

WIREs Mechanisms of Disease

View full text Add to dashboard Cite

The regulation of size and shape is a fundamental requirement of biological development and has been a subject of scientific study for centuries, but we still lack an understanding of how organisms know when to stop growing. Imaginal wing disks of the fruit fly Drosophila melanogaster, which are precursors of the adult wings, are an archetypal tissue for studying growth control. The growth of the disks is dependent on many inter‐ and intra‐organ factors such as morphogens, mechanical forces, nutrient levels, and hormones that influence gene expression and cell growth. Extracellular signals are transduced into gene‐control signals via complex signal transduction networks, and since cells typically receive many different signals, a mechanism for integrating the signals is needed. Our understanding of the effect of morphogens on tissue‐level growth regulation via individual pathways has increased significantly in the last half century, but our understanding of how multiple biochemical and mechanical signals are integrated to determine whether or not a cell decides to divide is still rudimentary. Numerous fundamental questions are involved in understanding the decision‐making process, and here we review the major biochemical and mechanical pathways involved in disk development with a view toward providing a basis for beginning to understand how multiple signals can be integrated at the cell level, and how this translates into growth control at the level of the imaginal disk. This article is categorized under: Analytical and Computational Methods > Computational Methods Biological Mechanisms > Cell Signaling Models of Systems Properties and Processes > Cellular Models

show abstract

Section: A Model For the Control Of Disk Sizementioning

confidence: 99%

Growth control in the Drosophila wing disk

Gou

Stotsky

Othmer

2020

WIREs Mechanisms of Disease

View full text Add to dashboard Cite

show abstract

“…Cells must change shape and move but need to do so without disrupting tissue integrity. These paired needs require integration of the cell adhesion and actomyosin cytoskeletal machinery, which work together to provide cells, tissues, and organs with the correct architecture and allow them to change shape and move in coordinated ways (Heer and Martin, 2017). Epithelial cells, a polarized cell type that act as the building blocks for most tissues, must coordinate adhesion and the cytoskeleton during tissue development.…”

Section: Introductionmentioning

confidence: 99%

The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

Manning

Perez-Vale

Schaefer

et al. 2019

Preprint

View full text Add to dashboard Cite

During morphogenesis cells must change shape and move without disrupting tissue integrity. This requires cell-cell junctions to allow dynamic remodeling while resisting force generated by the actomyosin cytoskeleton. Multiple proteins play roles in junctional-cytoskeletal linkage, but the mechanisms by which they act remain unclear. Drosophila Canoe maintains adherens junction-cytoskeletal linkage during gastrulation.Canoe's mammalian homolog Afadin plays similar roles in cultured cells, working in parallel with ZO-1 proteins, particularly at multicellular junctions. We took these insights back into the fly embryo, exploring how cells maintain epithelial integrity when challenged by adherens junction remodeling during germband extension and dorsal closure. We found Canoe helps cells maintain junctional-cytoskeletal linkage when challenged by the junctional remodeling inherent in mitosis, cell intercalation and neuroblast invagination, or by forces generated by the actomyosin cable at the leading edge. However, even in the absence of Canoe many cells retain epithelial integrity. This is explained by a parallel role played by the ZO-1 homolog Polychaetoid. In embryos lacking both Canoe and Polychaetoid, cell junctions fail early, with multicellular junctions especially sensitive, leading to widespread loss of epithelial integrity. Our data suggest Canoe and Polychaetoid stabilize Bazooka/Par3 at cell-cell junctions, helping maintain balanced apical contractility and tissue integrity.

show abstract

“…This common effect suggested that changes in caveola abundance can set levels of tissue tension in monolayers. Changes in cellular contractility are commonly thought to arise when signals such as MLCK and RhoA-ROCK alter the activity of Myosin II (Heer and Martin, 2017). However, neither the level nor activity of 13 Myosin II was detectably changed in CAV1 KD cells.…”

Section: Discussionmentioning

confidence: 99%

Caveolae set levels of epithelial monolayer tension to eliminate tumor cells

Teo

Gómez

Noordstra

et al. 2019

Preprint

View full text Add to dashboard Cite

Mechanical tension governs epithelial morphogenesis and homeostasis, but its regulation remains poorly understood. Tension is commonly contractile, arising when the actomyosin cortices of cells are mechanically coupled together by cadherin adhesion. Here we report that caveolae control levels of epithelial tension and show that this is necessary for oncogene-transfected cells to be eliminated by apical extrusion. Depletion of caveolin-1 (CAV1) in the surrounding epithelium, but not in the oncogene-expressing cells, blocked extrusion leading to the retention and proliferation of transformed cells within the monolayer. Tensile stress was aberrantly elevated in CAV1-depleted monolayers due to elevated levels of phosphoinositide-4,5-bisphosphate (PtdIns(4,5)P 2 ) causing increased recruitment of the formin, FMNL2. Oncogenic extrusion was restored to CAV1-deficient monolayers when tension was corrected by depleting FMNL2, blocking PtdIns(4,5)P 2 , or disabling the interaction between FMNL2 and PtdIns(4,5)P 2 . Thus, by controlling lipid signalling to the actin cytoskeleton, caveolae regulate mechanical tension for epithelial homeostasis.

show abstract

Tension, contraction and tissue morphogenesis

Cited by 177 publications

References 131 publications

Growth control in the Drosophila wing disk

Growth control in the Drosophila wing disk

The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

Caveolae set levels of epithelial monolayer tension to eliminate tumor cells

Contact Info

Product

Resources

About