Structural Redundancy in Supracellular Actomyosin Networks Enables Robust Tissue Folding

Yevick, Hannah; Miller, Pearson W.; Dunkel, Jörn; Martin, Adam C.

doi:10.1016/j.devcel.2019.06.015

Cited by 71 publications

(73 citation statements)

References 56 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The rescue mechanism relies on a buildup of a strong precursor stress in the disrupted zones. An analysis of constriction patterns in live embryos in which contractile force transmission has been reduced locally using optogenetic techniques [24] is consistent with our theoretical findings and consistent with the recent findings of others [16,25]. We thus conclude that mechanical feedback and the associated formation of cellular constriction chains reduce nonuniformities of the constriction pattern and aid robustness of the VFF in the…”

Section: Introductionsupporting

confidence: 91%

“…Instead, entire apical cell ends are represented as mechanically coupled, stress-responsive active particles that are capable of random constrictions. This coarse-grained AGF technique can readily describe populations of cell membranes, adherens junctions, the cortical apical actomyosin meshwork, actomyosin rings at the cell junction, and supracellular actomyosin filaments [16,21,25]. A typical vertex model likely would be inadequate for description of this system, whereas a particle-based model that treats cells as undivided entities described by their effective properties is more appropriate.…”

Section: The Epithelial Blastoderm Can Be Represented As a System Of mentioning

confidence: 99%

See 1 more Smart Citation

Mechanical feedback and robustness of apical constrictions inDrosophilaembryo ventral furrow formation

Holcomb

Gao

Servati

et al. 2019

Preprint

View full text Add to dashboard Cite

The key process giving rise to ventral furrow formation (VFF) in the Drosophila embryo 14 is apical (outer side) constriction of cells in the ventral region. A combined effect of the cellular 15 constrictions is a negative spontaneous curvature of the cell layer, which buckles inwards. In our 16 recent paper [Gao et al. (2016). J Phys Condens Matter, 28(41), 414021] we showed that the cell 17 constrictions in the initial phase of VFF produce well-defined cellular constriction chain (CCC) 18 patterns, and we argued that CCC formation is a signature of mechanical signaling that coordinates 19 apical constrictions through tensile stress. In the present study, we provide a statistical comparison 20 between our active granular fluid (AGF) model and time lapses of live embryos. We also 21 demonstrate that CCCs can penetrate regions of reduced constriction probability, and we argue 22 that CCC formation increases robustness of VFF to spatial variation of cell contractility. 23 24 128 determine the essential features of the geometry of constriction patterns without considering 129 complexities of temporal aspects of constrictions of individual cells. 130 The AGF model predicts that tensile-stress feedback between constricting cells re-131 sults in formation of CCCs 132 Description of the AGF model 133 6 of 28

show abstract

Section: Introductionsupporting

confidence: 91%

Section: The Epithelial Blastoderm Can Be Represented As a System Of mentioning

confidence: 99%

Mechanical feedback and robustness of apical constrictions inDrosophilaembryo ventral furrow formation

Holcomb

Gao

Servati

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Junctions transmit these forces through interactions with the actomyosin cytoskeleton which in turn influence the behavior of adherens junctions ( Weng and Wieschaus, 2016 ). These interactions ultimately generate the supracellular actomyosin network observed during ventral furrow formation ( Martin et al, 2010 ; Yevick et al, 2019 ). In our experiments, ectopic Rho1 activation was not sufficient to induce such networks in the dorsal epithelium, indicating a requirement for ventral-specific factors in their assembly.…”

Section: Discussionmentioning

confidence: 99%

“…Together with Concertina, a maternally contributed G α protein, and Smog, a maternally contributed GPCR, these factors recruit and activate RhoGEF2, a Rho1-specific guanine nucleotide exchange factor, at the apical membrane of ventral cells ( Parks and Wieschaus, 1991 ; Kölsch et al, 2007 ; Nikolaidou and Barrett, 2004 ; Kerridge et al, 2016 ). RhoGEF2 then activates Rho1 to assemble a contractile actomyosin network ( Fox and Peifer, 2007 ); these networks within single cells are coupled through adherens junctions between neighboring cells into a supracellular actomyosin network that promotes apical constriction and robust ventral furrow formation ( Martin et al, 2010 ; Yevick et al, 2019 ). Notably, both RhoGEF2 accumulation and Rho1 activation are pulsatile ( Martin et al, 2010 ; Mason et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Rho1 activation recapitulates early gastrulation events in the ventral, but not dorsal, epithelium ofDrosophilaembryos

Rich

Fehon

Glotzer

2020

Preprint

View full text Add to dashboard Cite

Ventral furrow formation, the first step in Drosophila gastrulation, is a well-studied 9 example of tissue morphogenesis. Rho1 is highly active in a subset of ventral cells and is required 10 for this morphogenetic event. However, it is unclear whether spatially patterned Rho1 activity 11 alone is sufficient to recapitulate all aspects of this morphogenetic event, including anisotropic 12 apical constriction and coordinated cell movements. Here, using an optogenetic probe that rapidly 13 and robustly activates Rho1 in Drosophila tissues, we show that Rho1 activity induces ectopic 14 deformations in the dorsal and ventral epithelia of Drosophila embryos. These perturbations reveal 15 substantial differences in how ventral and dorsal cells, both within and outside the zone of Rho1 16 activation, respond to spatially and temporally identical patterns of Rho1 activation. Our results 17 demonstrate that an asymmetric zone of Rho1 activity is not sufficient to recapitulate ventral 18 furrow formation and indicate that additional, ventral-specific factors contribute to the cell-and 19 tissue-level behaviors that emerge during ventral furrow formation. 20 21 30 Ventral furrow formation in the Drosophila embryo is one of the best studied examples of tissue 31 morphogenesis; it is the first step in Drosophila gastrulation. Ventral furrow formation occurs when 32 a rectangular zone of approximately 1000 cells, arranged in 18 rows, on the ventral surface of the 33 embryonic epithelium apically constrict and invaginate into the embryo, ultimately giving rise to 34 the embryonic mesoderm (Leptin and Grunewald, 1990; Sweeton et al., 1991). Many molecules 35 required for ventral furrow formation have been identified: An extracellular serine protease cascade 36 activates the transcription factor Dorsal which drives the expression of two additional transcription 37 factors, Snail and Twist, in a subset of ventral cells, inducing them to adopt mesodermal fates 38 (Morisato and Anderson, 1995; Ip et al., 1992; Jiang et al., 1991). Snail and Twist then induce the 39 1 of 24 Manuscript submitted to eLife expression of secreted and cell surface molecules, including the ligand Fog, the G-protein-coupled 40 receptor (GPCR) Mist, and the transmembrane protein T48 (Dawes-Hoang et al., 2005; Costa et al., 41 1994; Kölsch et al., 2007; Manning et al., 2013). Together with Concertina, a maternally contributed 42 G protein, and Smog, a maternally contributed GPCR, these factors recruit and activate RhoGEF2, 43 a Rho1-specific guanine nucleotide exchange factor, at the apical membrane of ventral cells (Parks 44 and Wieschaus, 1991; Kölsch et al., 2007; Nikolaidou and Barrett, 2004; Kerridge et al., 2016). 45 RhoGEF2 then activates Rho1 to assemble a contractile actomyosin network (Fox and Peifer, 2007); 46 these networks within single cells are coupled through adherens junctions between neighboring 47 Addressing these and related questions necessitates the ability to activate Rho1 with high spatial 74 and temporal precision witho...

show abstract

“…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

View full text Add to dashboard Cite

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

show abstract

Structural Redundancy in Supracellular Actomyosin Networks Enables Robust Tissue Folding

Cited by 71 publications

References 56 publications

Mechanical feedback and robustness of apical constrictions inDrosophilaembryo ventral furrow formation

Mechanical feedback and robustness of apical constrictions inDrosophilaembryo ventral furrow formation

Rho1 activation recapitulates early gastrulation events in the ventral, but not dorsal, epithelium ofDrosophilaembryos

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

Contact Info

Product

Resources

About