Integration of actomyosin contractility with cell-cell adhesion during dorsal closure

Duque, Julia; Gorfinkiel, Nicole

doi:10.1242/dev.136127

Cited by 22 publications

(33 citation statements)

References 43 publications

(67 reference statements)

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“…, 2011; Levayer and Lecuit, 2013; Duque and Gorfinkiel, 2016). We therefore investigated cadherin-mediated adhesion in mys −/− mutants (Figure 2).…”

Section: Resultsmentioning

confidence: 99%

Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure

Goodwin

Lostchuck

Cramb

et al. 2017

MBoC

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“…, 2011; Levayer and Lecuit, 2013; Duque and Gorfinkiel, 2016). We therefore investigated cadherin-mediated adhesion in mys −/− mutants (Figure 2).…”

Section: Resultsmentioning

confidence: 99%

Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure

Goodwin

Lostchuck

Cramb

et al. 2017

MBoC

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“…The amnioserosa, an extra-embryonic tissue, covers the dorsal hole and contributes to ectodermal closure by providing contractile forces that pull the contralateral ectodermal sheets together [54, 57, 58]. DC requires DE-Cad-mediated adhesion for ectodermal migration and fusion [59, 60]. To analyze Raskol and DE-Cad dynamics, we conducted time-lapse live imaging of embryos expressing YFP-tagged Raskol and RFP-tagged DE-Cad during DC.…”

Section: Resultsmentioning

confidence: 99%

“…Here, Raskol colocalized with actin suggesting that it may play a role in actin dynamics. Since Raskol contains a GAP domain and colocalizes with the cortical actin cytoskeleton in BCs, the FE, the amnioserosa and the dorsal most ectodermal cells [55, 60], we sought to determine whether it functions to regulate actin organization in BCs. We stained egg chambers expressing raskol RNAi in the BCs under the control of slbo -GAL4 driver for F-actin (phalloidin) and nuclei (DAPI) to assess F-actin distribution in the migrating cluster.…”

Section: Resultsmentioning

confidence: 99%

Evolutionary rate covariation analysis of E-cadherin identifies Raskol as regulator of cell adhesion and actin dynamics inDrosophila

Raza

Choi

et al. 2018

Preprint

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The adherens junction couples the actin cytoskeletons of neighboring cells to provide the foundation for multicellular organization. The core of the adherens junction is the cadherin-catenin complex that arose early in the evolution of multicellularity to link cortical actin to intercellular adhesions. Over time, evolutionary pressures have shaped the signaling and mechanical functions of the adherens junction to meet specific developmental and physiological demands. Evolutionary rate covariation (ERC) identifies genes with correlated fluctuations in evolutionary rate that can reflect shared selective pressures and functions. Here we use ERC to identify genes with evolutionary histories similar to shotgun (shg), which encodes the Drosophila E-cadherin (DE-Cad) ortholog. Core adherens junction components α-catenin and p120-catenin displayed strong ERC correlations with shg, indicating that they evolved under similar selective pressures during evolution between Drosophila species. Further analysis of the shg ERC profile revealed a collection of genes not previously associated with shg function or cadherin-mediated adhesion. We then analyzed the function of a subset of ERC-identified candidate genes by RNAi during border cell (BC) migration and identified novel genes that function to regulate DE-Cad. Among these, we found that the gene CG42684, which encodes a putative GTPase activating protein (GAP), regulates BC migration and adhesion. We named CG42684 raskol (“to split” in Russian) and show that it regulates DE-Cad levels and actin protrusions in BCs. We propose that Raskol functions with DE-Cad to restrict Ras/Rho signaling and help guide BC migration. Our results demonstrate that a coordinated selective pressure has shaped the adherens junction and this can be leveraged to identify novel components of the complexes and signaling pathways that regulate cadherin-mediated adhesion.Author SummaryThe establishment of intercellular adhesions facilitated the genesis of multicellular organisms. The adherens junction, which links the actin cytoskeletons of neighboring cells, arose early in the evolution of multicellularity and selective pressures have shaped its function and molecular composition over time. In this study, we used evolutionary rate covariation (ERC) analysis to examine the evolutionary history of the adherens junction and to identify genes that coevolved with the adherens junction gene shotgun, which encodes the Drosophila E-cadherin (DE-Cad). ERC analysis of shotgun revealed a collection of genes with similar evolutionary histories. We then tested the role of these genes in border cell migration in the fly egg chamber, a process that requires the coordinated regulation of cell-cell adhesion and cell motility. Among these, we found that a previously uncharacterized gene CG42684, which encodes a putative GTPase activating protein (GAP), regulates the collective cell migration of border cells, stabilizes cell-cell adhesions and regulates the actin dynamics. Our results demonstrate that components of the adherens junction share an evolutionary history and that ERC analysis is a powerful method to identify novel components of cell adhesion complexes in Drosophila.

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“…It has been reported that the myosin activity in amnioserosa cells increases as dorsal closure proceeds (35), implying an enhanced amnioserosa contraction due to the increase in myosin activation coefficient α in Eq. 2 (38). To account for this biochemical feature, we gradually increase α while keeping the myosin deactivation rate β fixed.…”

Section: Resultsmentioning

confidence: 99%

Activation and synchronization of the oscillatory morphodynamics in multicellular monolayer

Lin

Lan

et al. 2017

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

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Oscillatory morphodynamics provides necessary mechanical cues for many multicellular processes. Owing to their collective nature, these processes require robustly coordinated dynamics of individual cells, which are often separated too distantly to communicate with each other through biomaterial transportation. Although it is known that the mechanical balance generally plays a significant role in the systems' morphologies, it remains elusive whether and how the mechanical components may contribute to the systems' collective morphodynamics. Here, we study the collective oscillations in the Drosophila amnioserosa tissue to elucidate the regulatory roles of the mechanical components. We identify that the tensile stress is the key activator that switches the collective oscillations on and off. This regulatory role is shown analytically using the Hopf bifurcation theory. We find that the physical properties of the tissue boundary are directly responsible for synchronizing the oscillatory intensity and polarity of all inner cells and for orchestrating the spatial oscillation patterns in the tissue.collective cell oscillations | morphodynamics | Hopf bifurcation M orphodynamics describes how a subject's form changes over time. In living systems, the morphodynamic changes are both the effect and the cause of coordinated biochemical and biophysical processes. On the one hand, a system's morphological changes result from intracellular force generation and intercellular force transmission through sequences of biological events. On the other hand, the morphodynamic changes provide various mechanical and physical cues that are critical for the morphogenesis of multicellular tissues (1, 2) and the development of organisms (3-5). Owing to the collective nature of many biological processes, it is of profound interest to understand the principle underlying the morphodynamics of a living thing that is built from individual yet coherent cells (6-8).Oscillatory morphodynamics is an important category of collective morphodynamic phenomena that exists in many biological systems, including vertebrate segmentation (9), mesoderm invagination (10), and germband extension (11). These morphological oscillations are rooted in the active contraction of the actomyosin cytoskeleton in individual cells (12)(13)(14)(15) and are often coupled with other intracellular biochemical signaling pathways (9,13,14). During the oscillatory process, the actomyosin cytoskeleton gets activated and forms an apical network beneath the membrane, which further facilitates the formation of cell-cell junctions that allow force transmission from a cell to its neighbors (16). These observations have motivated many modeling efforts that generally fall into two categories: The couplingbased models attempt to couple membrane tension with the actomyosin regulation pathway to reproduce the oscillation of single or multiple cells (14, 17); the input-based ratchet models treat the cortical actin-myosin cytoskeleton or the supracellular actin cable as a programed machine tha...

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Integration of actomyosin contractility with cell-cell adhesion during dorsal closure

Cited by 22 publications

References 43 publications

Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure

Cell–cell and cell–extracellular matrix adhesions cooperate to organize actomyosin networks and maintain force transmission during dorsal closure

Evolutionary rate covariation analysis of E-cadherin identifies Raskol as regulator of cell adhesion and actin dynamics inDrosophila

Activation and synchronization of the oscillatory morphodynamics in multicellular monolayer

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