Tissue-Scale Mechanical Coupling Reduces Morphogenetic Noise to Ensure Precision during Epithelial Folding

Eritano, Anthony S.; Bromley, Claire L.; Albero, Antonio Bolea; Schütz, Lucas; Wen, Fu-Lai; Takeda, Masaya; Fukaya, Takashi; Sami, Mustafa M.; Shibata, Tatsuo; Lemke, Steffen; Wang, Yu-Chiun

doi:10.1016/j.devcel.2020.02.012

Cited by 46 publications

(72 citation statements)

References 73 publications

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“…34 A role for mechanics in symmetrization of body plans extends beyond the bilateria, as demonstrated by the action of muscle contraction in recovery of radial symmtery in Cndaria. 35 Our work showing how tissue surface tension ensures precision of somite morphology joins recent studies of mechanical processes reported to buffer heterogeneous cell growth in sepals in plants 36 and to enable straight cephalic furrow formation in Drosophila embryonic epithelia, 37 revealing mechanics as a general principle in ensuring developmental precision.…”

Section: Apsupporting

confidence: 59%

Somite surface tension buffers imprecise segment lengths to ensure left-right symmetry

Naganathan

Popović

Oates

2020

Preprint

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The body axis of vertebrate embryos is periodically segmented into bilaterally symmetric pairs of somites. The anteroposterior length and boundary position of somites are thought to be molecularly determined prior to somite morphogenesis. We show that in zebrafish embryos, initial somite lengths and positions are imprecise and many somites form left-right asymmetrically. Yet, within an hour, lengths are adjusted, becoming more symmetric, through somite deformations occurring independently on the left and right sides of the embryo. This adjustment is directed by a combination of somite surface tension, external stresses from neighbouring tissues and convergence-extension flows within somites. The ensuing left-right symmetry in somite boundary positions follows as a straightforward consequence of the length adjustments. Thus, the precision and symmetry of a fundamental embryonic morphological pattern is ensured by tissue mechanics.

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Section: Apsupporting

confidence: 59%

Somite surface tension buffers imprecise segment lengths to ensure left-right symmetry

Naganathan

Popović

Oates

2020

Preprint

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“…Interestingly, two recent papers addressed the robustness of tissue invagination. While the work of Yevick et al highlights the importance of mechanical redundancy to resist to accidental damage (Yevick et al, 2019), Eritano et al reveal the role of mechanical coupling as an intrinsic property of morphogenesis to buffer small variability in gene expression patterns (Eritano et al, 2020). This study appears complementary to these previous works, showing how morphogenesis is naturally protected from mechanical perturbations occurring randomly in the surroundings, by creating a fence through Arp2/3-dependent junctional myosin II planar polarity.…”

Section: Discussionmentioning

confidence: 61%

“…On the one hand, Hong et al (Hong et al, 2018) proposed, based on theoretical modeling, that tissue mechanics could buffer the heterogeneity observed at a single-cell level in term of growth and stiffness. More recently, this idea has been tested experimentally and mechanical forces have been shown to buffer local heterogeneity both in zebrafish and in Drosophila (Akieda et al, 2019;Eritano et al, 2020). On the other hand, Yevick et al (Yevick et al, 2019) identified redundant mechanical networks involved in the construction of a particular shape.…”

Section: Introductionmentioning

confidence: 99%

Arp2/3-dependent mechanical control of morphogenetic robustness in an inherently challenging environment

et al. 2021

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Summary Epithelial sheets undergo highly reproducible remodeling to shape organs. This stereotyped morphogenesis depends on a well-defined sequence of events leading to the regionalized expression of developmental patterning genes that finally triggers downstream mechanical forces to drive tissue remodeling at a pre-defined position. However, how tissue mechanics controls morphogenetic robustness when challenged by intrinsic perturbations in close proximity has never been addressed. Using Drosophila developing leg, we show that a bias in force propagation ensures stereotyped morphogenesis despite the presence of mechanical noise in the environment. We found that knockdown of the Arp2/3 complex member Arpc5 specifically affects fold directionality while altering neither the developmental nor the force generation patterns. By combining in silico modeling, biophysical tools, and ad hoc genetic tools, our data reveal that junctional myosin II planar polarity favors long-range force channeling and ensures folding robustness, avoiding force scattering and thus isolating the fold domain from surrounding mechanical perturbations.

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“…In the context of the NE-to-NSC transition, NE cells presumably read their distance to the NSC front through a combination of EGFR and Notch signalling to regulate L'sc, but how EGFR and Notch contribute to the precise temporal and spatial dynamics of L'sc remains to be studied. The other involves tissue-scale mechanical coupling to organize cells in space in a reproducible manner (Eritano et al, 2020;Aliee et al, 2012;Yevick et al, 2019). For example, neural progenitors in the fish neural tube rearrange cellcell contacts to establish sharp boundary through cell sorting.…”

Section: Discussionmentioning

confidence: 99%

Neuralized regulates a travelling wave of Epithelium-to-Neural Stem Cell morphogenesis inDrosophila

Shard

Luna-Escalante

Schweisguth

2020

Preprint

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Many tissues are produced during development by specialized progenitor cells emanating from epithelia via an Epithelial-to-Mesenchymal Transition (EMT). Most studies have so far focused on cases involving single or isolated groups of cells. Here we describe an EMT-like process that requires tissue level coordination. This EMT-like process occurs along a continuous front in the Drosophila optic lobe neuroepithelium to produce neural stem cells (NSCs). We find that emerging NSCs remain epithelial and apically constrict before dividing asymmetrically to produce neurons. Apical constriction is associated with contractile myosin pulses and requires the E3 ubiquitin ligase Neuralized and RhoGEF3. Neuralized downregulates the apical protein Crumbs via its interaction with Stardust. Disrupting the regulation of Crumbs by Neuralized led to defects in apical constriction and junctional myosin accumulation, and to imprecision in the integration of emerging NSCs into the transition front. Neuralized therefore appears to mechanically couple NSC fate acquisition with cell-cell rearrangement to promote smooth progression of the differentiation front. excitable reaction-diffusion mechanism. Accordingly, an activator signal, the Epidermal Growth Factor (EGF) Spitz, spreads in the NE by diffusion and self-induction and triggers a negative feed-back via the production of a non-diffusible inhibitor, i.e. the proneural factor Lethal of scute (L'sc) that inhibits the production of active Spitz by promoting NE-to-NSC

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Tissue-Scale Mechanical Coupling Reduces Morphogenetic Noise to Ensure Precision during Epithelial Folding

Cited by 46 publications

References 73 publications

Somite surface tension buffers imprecise segment lengths to ensure left-right symmetry

Somite surface tension buffers imprecise segment lengths to ensure left-right symmetry

Arp2/3-dependent mechanical control of morphogenetic robustness in an inherently challenging environment

Neuralized regulates a travelling wave of Epithelium-to-Neural Stem Cell morphogenesis inDrosophila

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