Control of cell flattening and junctional remodeling during squamous epithelial morphogenesis in<i>Drosophila</i>

Pope, Karen L.; Harris, Tony

doi:10.1242/dev.019802

Cited by 82 publications

(116 citation statements)

References 44 publications

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“…We conclude that apical constriction-induced basal movement of cytoplasm and volume conservation are the key factors that control both cell lengthening and the nucleus movement. This mechanism differs from previously proposed mechanisms ascribing to microtubules a central role in controlling cell length in epithelial cells (18), fibroblasts (19), and myoblasts (17) as well as nucleus movement (20). Volume conservation seems to be an effective means for localized subcellular force-generating machineries to affect shape changes in much larger structures across entire cells and tissues.…”

Section: Discussioncontrasting

confidence: 99%

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Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis

Gelbart

Martin

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

131

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Tissue morphogenesis is the process in which coordinated movements and shape changes of large numbers of cells form tissues, organs, and the internal body structure. Understanding morphogenetic movements requires precise measurements of whole-cell shape changes over time. Tissue folding and invagination are thought to be facilitated by apical constriction, but the mechanism by which changes near the apical cell surface affect changes along the entire apical-basal axis of the cell remains elusive. Here, we developed Embryo Development Geometry Explorer, an approach for quantifying rapid whole-cell shape changes over time, and we combined it with deep-tissue time-lapse imaging based on fast two-photon microscopy to study Drosophila ventral furrow formation. We found that both the cell lengthening along the apical-basal axis and the movement of the nucleus to the basal side proceeded stepwise and were correlated with apical constriction. Moreover, cell volume lost apically due to constriction largely balanced the volume gained basally by cell lengthening. The volume above the nucleus was conserved during its basal movement. Both apical volume loss and cell lengthening were absent in mutants showing deficits in the contractile cytoskeleton underlying apical constriction. We conclude that a single mechanical mechanism involving volume conservation and apical constriction-induced basal movement of cytoplasm accounts quantitatively for the cell shape changes and the nucleus movement in Drosophila ventral furrow formation. Our study provides a comprehensive quantitative analysis of the fast dynamics of whole-cell shape changes during tissue folding and points to a simplified model for Drosophila gastrulation.two-photon imaging | 4D reconstruction | segmentation

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Section: Discussioncontrasting

confidence: 99%

“…1C, Left). However, alternative scenarios seem plausible, in which separate, albeit sufficiently concerted, active cellular processes drive the sequence of apical and basal cell shape changes (16)(17)(18)(19) and the relocation of the nucleus (20,21) (Fig. 1C, Right).…”

mentioning

confidence: 99%

Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis

Gelbart

Martin

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

131

124

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“…As depletion of PIP3 did not block actomyosin cable assembly, loss of Baz must also trigger a PIP3-independent pathway that drives cable assembly. Baz exhibits a reciprocal distribution to actomyosin in other processes in the Drosophila embryo, including germband extension and amnioserosa remodelling; however, the molecular basis of this reciprocal relationship is not well understood, although recent work has indicated that Rho-kinase is involved (Pope and Harris, 2008;Simões et al, 2010;Zallen and Wieschaus, 2004).…”

Section: Discussionmentioning

confidence: 99%

Par3/Bazooka and phosphoinositides regulate actin protrusion formation during Drosophila dorsal closure and wound healing

et al. 2013

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SUMMARYEffective wound closure mechanisms are essential for maintenance of epithelial structure and function. The repair of wounded epithelia is primarily driven by the cells bordering the wound, which become motile after wounding, forming dynamic actin protrusions along the wound edge. The molecular mechanisms that trigger wound edge cells to become motile following tissue damage are not well understood. Using wound healing and dorsal closure in Drosophila, we identify a direct molecular link between changes in cell-cell adhesion at epithelial edges and induction of actin protrusion formation. We find that the scaffolding protein Par3/Bazooka and the lipid phosphatase Pten are specifically lost from cell-cell junctions at epithelial edges. This results in a localized accumulation of phosphatidylinositol 3,4,5-trisphosphate (PIP3), which promotes the formation of actin protrusions along the epithelial edge. Depleting PIP3 results in defective epithelial closure during both dorsal closure and wound healing. These data reveal a novel mechanism that directly couples loss of epithelial integrity to activation of epithelial closure.

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“…Apical constrictions of the amnioserosa also generate ratchet-like pulling forces on the actin cables of the lateral epidermis that move the epithelial sheets towards each other (Solon et al, 2009). The initially columnar amnioserosa cells flatten and elongate by reorienting their internal microtubules, and these dynamic cytoskeletally driven cell shape changes are crucial for the tissue closure process to proceed efficiently and smoothly (Pope and Harris, 2008). Interestingly, microtubules resist significant compressive forces in adult mammalian cells (Brangwynne et al, 2006), and by resisting actomyosin-based tensile forces via a tensegrity mechanism, they contribute to the control of the cytoskeletal prestress that maintains cell shape stability in embryonic and adult tissues and organs (reviewed by Ingber, 2006).…”

Section: Tissue Folding Invagination and Dorsal Closurementioning

confidence: 99%

Mechanical control of tissue and organ development

2010

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Many genes and molecules that drive tissue patterning during organogenesis and tissue regeneration have been discovered. Yet, we still lack a full understanding of how these chemical cues induce the formation of living tissues with their unique shapes and material properties. Here, we review work based on the convergence of physics, engineering and biology that suggests that mechanical forces generated by living cells are as crucial as genes and chemical signals for the control of embryological development, morphogenesis and tissue patterning. Key words: Cytoskeleton, Mechanical signaling, Morphogenesis, Pattern formation, Tension IntroductionWe now know many genes, morphogens and signaling molecules that govern tissue genesis. However, we do not fully understand how these chemical cues drive the formation of living tissues and organs with specialized forms and unique physical properties (e.g. rigidity, elastic recoil or viscoelasticity) required to pump blood, withstand repetitive movements or lift our bodies up against the force of gravity. A century ago, much of developmental control was explained in mechanical terms. In his classic treatise On Growth and Form, D'Arcy Thompson described how patterns are "diagrams of underlying forces" (Thompson, 1917). This is because a change in the three-dimensional (3D) shape of any structure, including living cells and tissues, must, at some level, result from the action of a force acting on a mass. Although this view was pushed aside by the advance of molecular biology, the relationship between physicality and developmental control is now coming into focus once again as a result of powerful new alliances between biologists, geneticists, engineers and physicists. This interdisciplinary approach has led to the discovery of fundamental links between mechanical forces, molecular biochemistry, gene expression and tissue patterning that drive embryogenesis and play a central role in morphogenesis and tissue maintenance throughout the life of an organism.In this article, we highlight some of the recent advances in this emerging field of mechanical biology. In particular, we focus on the role of mechanical forces that are generated in the contractile actin cytoskeleton of living cells and that act on the adhesions of these cells to neighboring cells and to the extracellular matrix (ECM). We describe how both traction forces exerted locally by single cells and more generalized forces (e.g. fluid shear, hydrostatic pressure) resulting from tension generated within the cytoskeletons of large groups of cells in tissues and organs are central to the control of tissue pattern formation during virtually all stages of embryogenesis.We also explore how mechanical signals are converted into changes in intracellular biochemistry and gene expression so that they influence fundamental mechanisms of cell fate determination and morphogenetic control that are also controlled by genes, soluble morphogens and chemical factors. Mechanical forces in early developmentThe shaping of the living embryo...

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Control of cell flattening and junctional remodeling during squamous epithelial morphogenesis inDrosophila

Cited by 82 publications

References 44 publications

Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis

Volume conservation principle involved in cell lengthening and nucleus movement during tissue morphogenesis

Par3/Bazooka and phosphoinositides regulate actin protrusion formation during Drosophila dorsal closure and wound healing

Mechanical control of tissue and organ development

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