Remodeling Tissue Interfaces and the Thermodynamics of Zipping during Dorsal Closure in Drosophila

Lu, Heng; Sokolow, Adam; Kiehart, Daniel P.; Edwards, Glenn S.

doi:10.1016/j.bpj.2015.10.017

Cited by 12 publications

(27 citation statements)

References 47 publications

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“…The fast phase, as observed in vivo, introduces two new factors into the closure of the AS tissue. The first is zippering (20)(21)(22), which occurs when filopodia are extended from one epidermis to the other and exert a pulling force to move the two leading edges toward each other. Filopodia are approximately 10 µm in length, and function only after the internal actomyosin contraction has brought the leading edges to within one or two cell widths.…”

Section: Fast Phase: Closurementioning

confidence: 99%

“…The advent of the fast phase brings a few new factors. As the AS tissue narrows, the opposing epidermis extends filopodia onto the opposite side, which then pull to help the closure (20)(21)(22). This is known as zippering.…”

mentioning

confidence: 99%

“…Ducuing and Vincent (19) reported that the actin cable does not contribute appreciably to the dorsal-ward movement of the leading edges.Thus, a consensus seems to be forming on a secondary role for the actin cable.The advent of the fast phase brings a few new factors. As the AS tissue narrows, the opposing epidermis extends filopodia onto the opposite side, which then pull to help the closure (20)(21)(22). This is known as zippering.…”

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confidence: 99%

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Dynamics of PAR proteins explain the oscillation and ratcheting mechanisms in dorsal closure

Durney

Harris

Feng

2018

Preprint

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We present a vertex-based model for Drosophila dorsal closure that predicts the mechanics of cell oscillation and contraction from the dynamics of the PAR proteins. Based on experimental observations of how aPKC, Par-6 and Bazooka migrate from the circumference of the apical surface to the medial domain, and how they interact with each other and ultimately regulate the apicomedial actomyosin, we formulate a system of differential equations that capture the key features of the process. The oscillation in cell area in the early phase of dorsal closure results from an intracellular negative feedback loop that involves myosin, an actomyosin regulator, aPKC and Bazooka. In the slow phase, gradual sequestration of apicomedial aPKC into Bazooka clusters causes incomplete disassembly of the myosin network over each cycle of oscillation, thus producing the so-called ratchet. The fast phase of rapid cell and tissue contraction arises when medial myosin, no longer hindered by aPKC, builds up in time and produces sustained contraction. Thus, a minimal set of rules governing the dynamics of the PAR proteins, extracted from experimental observations, can account for all major mechanical outcomes of dorsal closure, including the transitions between its three distinct phases.Insert Received for publication Date and in final form Date. 2 4 minutes (1,(4)(5)(6). The cell contracts following the assembly of the actomyosin network, and relaxes when the network disassembles (4, 7). After each cycle, the cell area returns to more or less the previous state. The contraction of one cell pulls on its neighbors, yielding a preference for antiphase pulsing between neighboring cells (1). But Blanchard et al. (3) have also observed transient "ribbons" of cells that are simultaneously contracting or expanding. It remains to be ascertained whether the oscillatory behavior originates from the autonomous dynamics within each cell or from the communications between neighbors, or even both (1,8,9).Naturally one seeks an explanation for the oscillatory behavior from biochemical signaling (4, 10-13). David et al. (4) highlighted the roles of the PAR proteins. Bazooka (Baz) promotes the duration of actomyosin contraction, while the Par-6/aPKC complex promotes the lull time between contractions. More recently, David et al. (12) further delineated the spatial and temporal relationship among the PAR proteins and the actomyosin network that periodically assembles in the apicomedial domain of the AS cells. The actomyosin recruits aPKC from the circumference of the apical surface toward the medial region, where it forms puncta that colocalize with the actomyosin network. In turn, aPKC recruits Bazooka into the medial region. As aPKC is known to inhibit actomyosin, and the formation and stabilization of aPKC-Baz complexes result in apical constriction, David et al. (12) hypothesized that the PAR proteins form a negative feedback loop with the medial actomyosin network to produce the oscillatory outcome. This is the strongest evidence so far in favor of a ...

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Section: Fast Phase: Closurementioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Dynamics of PAR proteins explain the oscillation and ratcheting mechanisms in dorsal closure

Durney

Harris

Feng

2018

Preprint

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“…Such coordination is a key feature of embryonic epithelia in which cells and tissues deform while tightly adhering to their neighbors. Coordinated cellular forces have been studied and modeled for several episodes of epithelial development in Drosophila melanogaster embryos, including ventral furrow invagination (4)(5)(6)(7)(8)(9)(10)(11)(12), germband extension (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26), and dorsal closure (27)(28)(29)(30)(31)(32)(33)(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46). More recently, studies have begun to elucidate the cellular forces driving another major episode of Drosophila embryogenesis known as germband retraction (2,47,48).…”

Section: Introductionmentioning

confidence: 99%

Elongated cells drive morphogenesis in a surface-wrapped finite element model of germband retraction

McCleery¹,

Veldhuis²,

Brodland³

et al. 2018

Preprint

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During Drosophila embryogenesis, the germband first extends to curl around the posterior end of the embryo, and then retracts back; however, retraction is not simply the reversal of extension. At a tissue level, extension is coincident with ventral furrow formation, and at a cellular level, extension occurs via convergent cell neighbor exchanges in the germband while retraction involves only changes in cell shape. To understand how cell shapes, tissue organization and cellular forces drive germband retraction, we investigate this process using a whole-embryo, surface-wrapped cellular finite element model. This model represents two key epithelial tissuesamnioserosa and germbandas adjacent sheets of 2D cellular finite elements that are wrapped around an ellipsoidal 3D approximation of an embryo. The model reproduces the detailed kinematics of in vivo retraction by fitting just one free model parameter, the tension along germband cell interfaces; all other cellular forces are constrained to follow ratios inferred from experimental observations. With no additional parameter adjustments, the model also reproduces failures of retraction when amnioserosa cells are removed to mimic U-shaped mutants or lasermicrosurgery experiments. Surprisingly, retraction in the model is robust to changes in cellular force values, but is critically dependent on starting from a configuration with highly elongated amnioserosa cells. Their extreme cellular elongation is established during the prior process of germband extension and is then used to drive retraction. The amnioserosa is the one tissue whose cellular morphogenesis is reversed in germband extension and retractionserving as a store of morphological information that coordinates the forces needed to retract the germband back to its pre-extension position and shape. In this case, and perhaps more generally, cellular force strengths are less important than the carefully established cell shapes that direct them.

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“…At each canthus, apposing leading edge cells are zipped together into a seam (Jacinto et al. , 2000; Lu et al. , 2015).…”

Section: Introductionmentioning

confidence: 99%

Quantifying dorsal closure in three dimensions

Sokolow

Kiehart

et al. 2016

MBoC

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The three-dimensional surface of dorsal-closure-staged Drosophila embryos is indented by two purse strings that surround an eye-shaped amnioserosa tissue. The amnioserosa forms a remarkably smooth, asymmetric dome that bulges outward due to the embryo’s internal pressure. Quantitative analysis with Laplace’s formula indicates that the elastic properties of the amnioserosa are isotropic and uniform.

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Remodeling Tissue Interfaces and the Thermodynamics of Zipping during Dorsal Closure in Drosophila

Cited by 12 publications

References 47 publications

Dynamics of PAR proteins explain the oscillation and ratcheting mechanisms in dorsal closure

Dynamics of PAR proteins explain the oscillation and ratcheting mechanisms in dorsal closure

Elongated cells drive morphogenesis in a surface-wrapped finite element model of germband retraction

Quantifying dorsal closure in three dimensions

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