<i>Drosophila</i>morphogenesis: Tissue force laws and the modeling of dorsal closure

Toyama, Yusuke; Yang, Guoqiang; Edwards, Glenn S.; Kiehart, Daniel P.; Venakides, Stephanos

doi:10.2976/1.3266062

Cited by 29 publications

(52 citation statements)

References 43 publications

(115 reference statements)

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“…This net force is the sum of positive contributions from the AS and purse string minus opposing forces in the LE (Hutson et al, 2003;Peralta et al, 2007;Toyama et al, 2008;Layton et al, 2009). In control injected embryos, closure occurs at a linear rate of 5.9±0.9 nm/s (n=7), consistent with published data for uninjected controls (Hutson et al, 2003;Peralta et al, 2007;Toyama et al, 2008) and corresponding to the 'fast phase' of closure reported by others (Gorfinkiel et al, 2009).…”

Section: Long-term Closure Defects Associated With Channel Inhibitionsupporting

confidence: 79%

“…Nevertheless, the rate of closure is nearly linear with time. In addition, removal of one contributing force by laser microsurgery leads to the upregulation of remaining forces, such that closure resumes at nearly unperturbed rates (Peralta et al, 2007;Layton et al, 2009). We hypothesize that mechanical feedback is involved in regulating closure in both native (non-laser perturbed) and experimentally manipulated embryos.…”

Section: Introductionmentioning

confidence: 99%

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Ion channels contribute to the regulation of cell sheet forces during Drosophila dorsal closure

Hunter¹,

Crawford²,

Genkins³

et al. 2014

Journal of Cell Science

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We demonstrate that ion channels contribute to the regulation of dorsal closure in Drosophila, a model system for cell sheet morphogenesis. We find that Ca 2+ is sufficient to cause cell contraction in dorsal closure tissues, as UV-mediated release of caged Ca 2+ leads to cell contraction. Furthermore, endogenous Ca 2+ fluxes correlate with cell contraction in the amnioserosa during closure, whereas the chelation of Ca 2+ slows closure. Microinjection of high concentrations of the peptide GsMTx4, which is a specific modulator of mechanically gated ion channel function, causes increases in cytoplasmic free Ca 2+ and actomyosin contractility and, in the long term, blocks closure in a dose-dependent manner. We identify two channel subunits, ripped pocket and dtrpA1 (TrpA1), that play a role in closure and other morphogenetic events. Blocking channels leads to defects in force generation via failure of actomyosin structures, and impairs the ability of tissues to regulate forces in response to laser microsurgery. Our results point to a key role for ion channels in closure, and suggest a mechanism for the coordination of force-producing cell behaviors across the embryo.

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Section: Long-term Closure Defects Associated With Channel Inhibitionsupporting

confidence: 79%

Section: Introductionmentioning

confidence: 99%

Ion channels contribute to the regulation of cell sheet forces during Drosophila dorsal closure

Hunter¹,

Crawford²,

Genkins³

et al. 2014

Journal of Cell Science

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“…At the same time, AS cells volume decreases, resulting in an additional contractile force promoting closure ( Figures 4C and S4A). Previous models have highlighted that an imbalance of tension is required for DC to proceed (Hutson et al, 2003;Layton et al, 2009). Here, we show that this imbalance of tension arises from temporal changes in the forces generated by the actin cable and by cell volume decrease.…”

Section: Discussionmentioning

confidence: 98%

Decrease in Cell Volume Generates Contractile Forces Driving Dorsal Closure

et al. 2015

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Biological tissues must generate forces to shape organs and achieve proper development. Such forces often result from the contraction of an apical acto-myosin meshwork. Here we describe an alternative mechanism for tissue contraction, based on individual cell volume change. We show that during Drosophila dorsal closure (DC), a wound healing-related process, the contraction of the amnioserosa (AS) is associated with a major reduction of the volume of its cells, triggered by caspase activation at the onset of the apoptotic program of AS cells. Cell volume decrease results in a contractile force that promotes tissue shrinkage. Estimating mechanical tensions with laser dissection and using 3D biophysical modeling, we show that the cell volume decrease acts together with the contraction of the actin cable surrounding the tissue to govern DC kinetics. Our study identifies a mechanism by which tissues generate forces and movements by modulating individual cell volume during development.

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“…We thank one of the anonymous referees for bringing to our attention the existence of the recent paper Layton et al (2009) where a so-called second generation model for DC is proposed. The main motivation of that work is quite similar to that of the present one; to develop a PDE generalization of the ODE model of Hutson et al (2003) that is applicable in more general settings.…”

Section: Introductionmentioning

confidence: 98%

A mathematical model for dorsal closure

Almeida

Bagnerini

Habbal

et al. 2011

Journal of Theoretical Biology

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During embryogenesis, drosophila embryos undergo epithelial folding and unfolding, which leads to a hole in the dorsal epidermis, transiently covered by an extraembryonic tissue called the amnioserosa. Dorsal closure (DC) consists of the migration of lateral epidermis towards the midline, covering the amnioserosa. It has been extensively studied since numerous physical mechanisms and signaling pathways present in DC are conserved in other morphogenetic events and wound healing in many other species (including vertebrates). We present here a simple mathematical model for DC that involves a reduced number of parameters directly linked to the intensity of the forces in the presence and which is applicable to a wide range of geometries of the leading edge (LE). This model is a natural generalization of the very interesting model proposed in Hutson et al. (2003). Being based on an ordinary differential equation (ODE) approach, the previous model had the advantage of being even simpler, but this restricted significantly the variety of geometries that could be considered and thus the number of modified dorsal closures that could be studied. A partial differential equation (PDE) approach, as the one developed here, allows considering much more general situations that show up in genetically or physically perturbed embryos and whose study will be essential for a proper understanding of the different components of the DC process. Even for native embryos, our model has the advantage of being applicable since an early stages of DC when there is no antero-posterior symmetry (approximately verified only in the late phases of DC). We validate our model in a native setting and also test it further in embryos where the zipping force is perturbed through the expression of spastin (a microtubule severing protein). We obtain variations of the force coefficients that are consistent with what was previously described for this setting.

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Drosophilamorphogenesis: Tissue force laws and the modeling of dorsal closure

Cited by 29 publications

References 43 publications

Ion channels contribute to the regulation of cell sheet forces during Drosophila dorsal closure

Ion channels contribute to the regulation of cell sheet forces during Drosophila dorsal closure

Decrease in Cell Volume Generates Contractile Forces Driving Dorsal Closure

A mathematical model for dorsal closure

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