Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis

Vasquez, Claudia G.; Tworoger, Michael; Martin, Adam C.

doi:10.1083/jcb.201402004

Cited by 149 publications

(215 citation statements)

References 72 publications

(121 reference statements)

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“…We find that dynamic motor activity is crucial for the stabilization of myosin at the cortex, consistent with recent work showing that myosin phosphorylation regulates contractility in epithelial morphogenesis (Kasza et al, 2014;Vasquez et al, 2014;Vasquez et al, 2016). Several actin regulators are sensitive to load, including formins (Courtemanche et al, 2013;Higashida et al, 2013;Jégou et al, 2013), and the filament-severing protein cofilin (Hayakawa et al, 2011;Tojkander et al, 2015).…”

Section: Results and Discussion Myosin Turnover Is Reduced Around Embsupporting

confidence: 75%

“…We investigated the role of phosphorylation on the stabilization of myosin at the wound border and tissue repair. We used embryos expressing GFP-tagged phosphomimetic (Sqh-AE, threonine-20 is mutated into an alanine and serine-21 is mutated into a glutamic acid), unphosphorylatable (Sqh-AA) or wild-type (Sqh-TS) forms of the MRLC (Vasquez et al, 2014) (Fig. 4A-E).…”

Section: Results and Discussion Myosin Turnover Is Reduced Around Embmentioning

confidence: 99%

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Tension regulates myosin dynamics during Drosophila embryonic wound repair

Kobb

Zulueta-Coarasa

Fernández-González

2017

Journal of Cell Science

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Embryos repair epithelial wounds rapidly in a process driven by collective cell movements. Upon wounding, actin and the molecular motor non-muscle myosin II are redistributed in the cells adjacent to the wound, forming a supracellular purse string around the lesion. Purse string contraction coordinates cell movements and drives rapid wound closure. By using fluorescence recovery after photobleaching in Drosophila embryos, we found that myosin turns over as the purse string contracts. Myosin turnover at the purse string was slower than in other actomyosin networks that had a lower level of contractility. Mathematical modelling suggested that myosin assembly and disassembly rates were both reduced by tension at the wound edge. We used laser ablation to show that tension at the purse string increased as wound closure progressed, and that the increase in tension was associated with reduced myosin turnover. Reducing purse string tension by laser-mediated severing resulted in increased turnover and loss of myosin. Finally, myosin motor activity was necessary for its stabilization around the wound and for rapid wound closure. Our results indicate that mechanical forces regulate myosin dynamics during embryonic wound repair.

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Section: Results and Discussion Myosin Turnover Is Reduced Around Embsupporting

confidence: 75%

Section: Results and Discussion Myosin Turnover Is Reduced Around Embmentioning

confidence: 99%

Tension regulates myosin dynamics during Drosophila embryonic wound repair

Kobb

Zulueta-Coarasa

Fernández-González

2017

Journal of Cell Science

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“…The formation of medial myosin pulses is dependent on a radialpolarized actin network with the pointed ends of actin filaments enriched in the medioapical region of ventral furrow cells (Coravos and Martin, 2016;Mason et al, 2013;Vasquez et al, 2014). Lowdose cytochalasin D (CytoD) treatment is a widely used method to disrupt the radial polarized apical actin network, and to block medial myosin pulses in ventral furrow cells (Coravos and Martin, 2016;Mason et al, 2013) and in cells undergoing shape deformation during Drosophila germband extension (Munjal et al, 2015).…”

Section: Medial Myosin Pulses Are Required For the Apical Constrictiomentioning

confidence: 99%

Apical constriction is driven by a pulsatile apical myosin network in delaminating Drosophila neuroblasts

Xue

Shaobo

et al. 2017

Development

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Cell delamination is a conserved morphogenetic process important for the generation of cell diversity and maintenance of tissue homeostasis. Here, we used Drosophila embryonic neuroblasts as a model to study the apical constriction process during cell delamination. We observe dynamic myosin signals both around the cell adherens junctions and underneath the cell apical surface in the neuroectoderm. On the cell apical cortex, the nonjunctional myosin forms flows and pulses, which are termed medial myosin pulses. Quantitative differences in medial myosin pulse intensity and frequency are crucial to distinguish delaminating neuroblasts from their neighbors. Inhibition of medial myosin pulses blocks delamination. The fate of a neuroblast is set apart from that of its neighbors by Notch signaling-mediated lateral inhibition. When we inhibit Notch signaling activity in the embryo, we observe that small clusters of cells undergo apical constriction and display an abnormal apical myosin pattern. Together, these results demonstrate that a contractile actomyosin network across the apical cell surface is organized to drive apical constriction in delaminating neuroblasts.

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“…Interestingly, both Rok and the Myosin binding subunit (Mbs) of Drosophila Myosin light chain phosphatase, colocalize with Myosin in dynamic medioapical foci in Drosophila epidermal cells and it has been suggested that actomyosin oscillations are an emergent property of a biomechanical network involving the regulators of Myosin phosphorylation and the movement -advection -of the actomyosin network (Munjal et al, 2015). Moreover, studies with phosphomimetic and a non-phosphorylatable forms of Myosin regulatory light chain [Spaghetti squash (Sqh), in Drosophila] have shown that altered Myosin phosphorylation dynamics perturbs actomyosin contractions and cell shape changes (Kasza et al, 2014;Munjal et al, 2015;Vasquez et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…Making use of Myosin mutant forms that substitute the phosphorylation site by unphosphorylatable and phosphomimetic residues (Jordan and Karess, 1997;Vasquez et al, 2014), we analyse how Myosin activity affects cell oscillations, cell contractility and tissue closure in the AS. Reducing Myosin activity prevents cell shape oscillations and reduces cell contractility.…”

Section: Introductionmentioning

confidence: 99%

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

Duque

Gorfinkiel

2016

Development

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In this work, we combine genetic perturbation, time-lapse imaging and quantitative image analysis to investigate how pulsatile actomyosin contractility drives cell oscillations, apical cell contraction and tissue closure during morphogenesis of the amnioserosa, the main force-generating tissue during the dorsal closure in Drosophila. We show that Myosin activity determines the oscillatory and contractile behaviour of amnioserosa cells. Reducing Myosin activity prevents cell shape oscillations and reduces cell contractility. By contrast, increasing Myosin activity increases the amplitude of cell shape oscillations and the time cells spend in the contracted phase relative to the expanded phase during an oscillatory cycle, promoting cell contractility and tissue closure. Furthermore, we show that in AS cells, Rok controls Myosin foci formation and Mbs regulates not only Myosin phosphorylation but also adhesion dynamics through control of Moesin phosphorylation, showing that Mbs coordinates actomyosin contractility with cell-cell adhesion during amnioserosa morphogenesis.

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Dynamic myosin phosphorylation regulates contractile pulses and tissue integrity during epithelial morphogenesis

Abstract: Dynamic regulation of Myo-II by Rho kinase and myosin phosphatase organizes contractile Myo-II pulses in both space and time, which is necessary to maintain tissue integrity during morphogenesis.

Cited by 149 publications

References 72 publications

Tension regulates myosin dynamics during Drosophila embryonic wound repair

Tension regulates myosin dynamics during Drosophila embryonic wound repair

Apical constriction is driven by a pulsatile apical myosin network in delaminating Drosophila neuroblasts

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

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