Downregulation of basal myosin‐
            <scp>II</scp>
            is required for cell shape changes and tissue invagination

Krueger, Daniel; Tardivo, Pietro; Nguyen, Congtin; Renzis, Stefano De

doi:10.15252/embj.2018100170

Cited by 69 publications

(59 citation statements)

References 41 publications

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“…As mesoderm cells achieve a more wedge-shaped morphology they undergo basal expansion and apical-basal shortening, which is correlated with basal myosin 2 depletion (Polyakov et al 2014). Indeed, ectopic myosin 2 activation after cell lengthening inhibits apical-basal cell shortening and tissue invagination, demonstrating a similarly important role for basal relaxation in cells achieving a final wedge shape and tissue invagination (Krueger et al 2018).…”

Section: Consequences Of Apical Constriction: Invagination Vs Ingresmentioning

confidence: 98%

The Physical Mechanisms ofDrosophilaGastrulation: Mesoderm and Endoderm Invagination

Martin

2020

Genetics

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A critical juncture in early development is the partitioning of cells that will adopt different fates into three germ layers: the ectoderm, the mesoderm, and the endoderm. This step is achieved through the internalization of specified cells from the outermost surface layer, through a process called gastrulation. In Drosophila, gastrulation is achieved through cell shape changes (i.e., apical constriction) that change tissue curvature and lead to the folding of a surface epithelium. Folding of embryonic tissue results in mesoderm and endoderm invagination, not as individual cells, but as collective tissue units. The tractability of Drosophila as a model system is best exemplified by how much we know about Drosophila gastrulation, from the signals that pattern the embryo to the molecular components that generate force, and how these components are organized to promote cell and tissue shape changes. For mesoderm invagination, graded signaling by the morphogen, Spätzle, sets up a gradient in transcriptional activity that leads to the expression of a secreted ligand (Folded gastrulation) and a transmembrane protein (T48). Together with the GPCR Mist, which is expressed in the mesoderm, and the GPCR Smog, which is expressed uniformly, these signals activate heterotrimeric G-protein and small Rho-family G-protein signaling to promote apical contractility and changes in cell and tissue shape. A notable feature of this signaling pathway is its intricate organization in both space and time. At the cellular level, signaling components and the cytoskeleton exhibit striking polarity, not only along the apical–basal cell axis, but also within the apical domain. Furthermore, gene expression controls a highly choreographed chain of events, the dynamics of which are critical for primordium invagination; it does not simply throw the cytoskeletal “on” switch. Finally, studies of Drosophila gastrulation have provided insight into how global tissue mechanics and movements are intertwined as multiple tissues simultaneously change shape. Overall, these studies have contributed to the view that cells respond to forces that propagate over great distances, demonstrating that cellular decisions, and, ultimately, tissue shape changes, proceed by integrating cues across an entire embryo.

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Section: Consequences Of Apical Constriction: Invagination Vs Ingresmentioning

confidence: 98%

The Physical Mechanisms ofDrosophilaGastrulation: Mesoderm and Endoderm Invagination

Martin

2020

Genetics

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“…Cell shape changes driven by contraction of cortical actomyosin filaments are of fundamental importance during animal development, underlying key morphogenetic processes such as cytokinesis (Pollard, 2010;Sedzinski et al, 2011), cell migration (Blanchoin et al, 2014), and localized remodeling of tissue shape (Bertet et al, 2004;Dawes-Hoang et al, 2005;Butler et al, 2009;Fernandez-Gonzalez et al, 2009;Heisenberg & Bellaiche, 2013;Izquierdo et al, 2018;Krueger et al, 2018). Fast in vivo imaging and in vitro studies demonstrate that contraction of cortical actomyosin networks is controlled by pulsatile flows of myosin-II molecules, which move centripetally as actin filaments contract and cell surface shrinks (Martin et al, 2009;Solon et al, 2009;Reymann et al, 2012;Banerjee et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

βH‐spectrin is required for ratcheting apical pulsatile constrictions during tissue invagination

et al. 2020

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Actomyosin-mediated apical constriction drives a wide range of morphogenetic processes. Activation of myosin-II initiates pulsatile cycles of apical constrictions followed by either relaxation or stabilization (ratcheting) of the apical surface. While relaxation leads to dissipation of contractile forces, ratcheting is critical for the generation of tissue-level tension and changes in tissue shape. How ratcheting is controlled at the molecular level is unknown. Here, we show that the actin crosslinker bH-spectrin is upregulated at the apical surface of invaginating mesodermal cells during Drosophila gastrulation. bH-spectrin forms a network of filaments which colocalize with medio-apical actomyosin fibers, in a process that depends on the mesoderm-transcription factor Twist and activation of Rho signaling. bH-spectrin knockdown results in non-ratcheted apical constrictions and inhibition of mesoderm invagination, recapitulating twist mutant embryos. bH-spectrin is thus a key regulator of apical ratcheting during tissue invagination, suggesting that actin cross-linking plays a critical role in this process.

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“…Tissue contraction can bring opposing cell sheets together, a mechanism used in both development and wound healing (Davidson et al, 2002;Kiehart et al, 2000). In addition, the selective contraction or expansion of one surface on an epithelial sheet (i.e., apical or basal) can result in tissue folding and cell invagination (Gutzman et al, 2008;Heer et al, 2017;Krueger et al, 2018;Polyakov et al, 2014;Sui et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Structural redundancy in supracellular actomyosin networks enables robust tissue folding

Yevick

Miller

Martin

2019

Preprint

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Tissue morphogenesis is strikingly reproducible. Yet, how tissues are robustly sculpted, even under challenging conditions, is unknown. Here, we combined network analysis, experimental perturbations, and computational modeling to determine how network connectivity between hundreds of contractile cells on the ventral side of the Drosophila embryo ensures robust tissue folding. We identified two network properties that mechanically promote robustness. First, redundant supracellular cytoskeletal network paths ensure global connectivity, even with network degradation. By forming many more connections than are required, morphogenesis is not disrupted by local network damage, analogous to the way redundancy guarantees the large-scale function of vasculature and transportation networks. Second, directional stiffening of edges oriented orthogonal to the folding axis promotes furrow formation at lower contractility levels. Structural redundancy and directional network stiffening ensure robust tissue folding with proper orientation.

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Downregulation of basal myosin‐ II is required for cell shape changes and tissue invagination

Cited by 69 publications

References 41 publications

The Physical Mechanisms ofDrosophilaGastrulation: Mesoderm and Endoderm Invagination

The Physical Mechanisms ofDrosophilaGastrulation: Mesoderm and Endoderm Invagination

βH‐spectrin is required for ratcheting apical pulsatile constrictions during tissue invagination

Structural redundancy in supracellular actomyosin networks enables robust tissue folding

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