scholarly journals Cell polarity determinant Dlg1 facilitates epithelial invagination by promoting tissue-scale mechanical coordination

2021 ◽  
Author(s):  
Melisa Andrea Fuentes ◽  
Bing He
Keyword(s):  
Laser Ablation ◽  
Cell Polarity ◽  
Cortical Actin ◽  
Multilayered Structures ◽  
Directed Movement ◽  
Apical Constriction ◽  
Mechanical Coupling ◽  
Apical Domain ◽  
Epithelial Sheets ◽  
Fundamental Mechanism

Epithelial folding mediated by apical constriction serves as a fundamental mechanism to convert flat epithelial sheets into multilayered structures. It remains elusive whether additional mechanical inputs are required for folding mediated by apical constriction. Using Drosophila mesoderm invagination as a model, we identified an important role for the non-constricting, lateral mesodermal cells adjacent to the constriction domain ("flanking cells") in facilitating epithelial folding. We found that depletion of the basolateral determinant, Dlg1, disrupts the transition between apical constriction and invagination without affecting the rate of apical constriction. Strikingly, the observed delay in invagination is associated with ineffective apical myosin contractions in the flanking cells that lead to overstretching of their apical domain. The defects in the flanking cells impede ventral-directed movement of the lateral ectoderm, suggesting reduced mechanical coupling between tissues. Specifically disrupting the flanking cells in wildtype embryos by laser ablation or optogenetic depletion of cortical actin is sufficient to delay the apical constriction-to-invagination transition. Our findings indicate that effective mesoderm invagination requires intact flanking cells and suggest a role for tissue-scale mechanical coupling during epithelial folding.

scholarly journals Jak-Stat pathway induces Drosophila follicle elongation by a gradient of apical contractility

2017 ◽  
Author(s):  
Hervé Alégot ◽  
Pierre Pouchin ◽  
Olivier Bardot ◽  
Vincent Mirouse
Keyword(s):  
Cell Polarity ◽  
Planar Cell Polarity ◽  
Myosin Ii ◽  
Cell Polarization ◽  
Follicular Epithelium ◽  
Morphogen Gradient ◽  
Apical Constriction ◽  
Activity Inhibition ◽  
Apical Domain ◽  
Stat Pathway

AbstractTissue elongation and its control by spatiotemporal signals is a major developmental question. Currently, it is thought that Drosophila ovarian follicular epithelium elongation requires the planar polarization of the basal domain cytoskeleton and of the extra-cellular matrix, associated with a dynamic process of rotation around the anteroposterior axis. Here we show, by careful kinetic analysis of fat2 mutants, that neither basal planar polarization nor rotation is required during a first phase of follicle elongation. Conversely, a JAK-STAT signaling gradient from each follicle pole orients early elongation. JAK-STAT controls apical pulsatile contractions, and Myosin II activity inhibition affects both pulses and early elongation. Early elongation is associated with apical constriction at the poles and oriented cell rearrangements, but without any visible planar cell polarization of the apical domain. Thus, a morphogen gradient can trigger tissue elongation via a control of cell pulsing and without planar cell polarity requirement.Impact StatementFollicle elongation does not rely solely on the basal side of the cells but also requires a mechanism integrating a developmental cue with a morphogenetic process involving their apical domain.

scholarly journals Jak-Stat pathway induces Drosophila follicle elongation by a gradient of apical contractility

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Hervé Alégot ◽  
Pierre Pouchin ◽  
Olivier Bardot ◽  
Vincent Mirouse
Keyword(s):  
Cell Polarity ◽  
Planar Cell Polarity ◽  
Myosin Ii ◽  
Cell Polarization ◽  
Follicular Epithelium ◽  
Morphogen Gradient ◽  
Apical Constriction ◽  
Activity Inhibition ◽  
Apical Domain ◽  
Stat Pathway

Tissue elongation and its control by spatiotemporal signals is a major developmental question. Currently, it is thought that Drosophila ovarian follicular epithelium elongation requires the planar polarization of the basal domain cytoskeleton and of the extra-cellular matrix, associated with a dynamic process of rotation around the anteroposterior axis. Here we show, by careful kinetic analysis of fat2 mutants, that neither basal planar polarization nor rotation is required during a first phase of follicle elongation. Conversely, a JAK-STAT signaling gradient from each follicle pole orients early elongation. JAK-STAT controls apical pulsatile contractions, and Myosin II activity inhibition affects both pulses and early elongation. Early elongation is associated with apical constriction at the poles and with oriented cell rearrangements, but without any visible planar cell polarization of the apical domain. Thus, a morphogen gradient can trigger tissue elongation through a control of cell pulsing and without a planar cell polarity requirement.

scholarly journals Filopodia formation and endosome clustering induced by mutant plus-end–directed myosin VI

2017 ◽  
Vol 114 (7) ◽  
pp. 1595-1600 ◽  
Author(s):  
Thomas A. Masters ◽  
Folma Buss
Keyword(s):  
Actin Filaments ◽  
Leucine Zipper ◽  
Adaptor Protein ◽  
Cell Cortex ◽  
Myosin Vi ◽  
Actin Network ◽  
Ph Domain ◽  
Cortical Actin ◽  
Directed Movement ◽  
Interacting Protein

Myosin VI (MYO6) is the only myosin known to move toward the minus end of actin filaments. It has roles in numerous cellular processes, including maintenance of stereocilia structure, endocytosis, and autophagosome maturation. However, the functional necessity of minus-end–directed movement along actin is unclear as the underlying architecture of the local actin network is often unknown. To address this question, we engineered a mutant of MYO6, MYO6+, which undergoes plus-end–directed movement while retaining physiological cargo interactions in the tail. Expression of this mutant motor in HeLa cells led to a dramatic reorganization of cortical actin filaments and the formation of actin-rich filopodia. MYO6 is present on peripheral adaptor protein, phosphotyrosine interacting with PH domain and leucine zipper 1 (APPL1) signaling endosomes and MYO6+ expression causes a dramatic relocalization and clustering of this endocytic compartment in the cell cortex. MYO6+ and its adaptor GAIP interacting protein, C terminus (GIPC) accumulate at the tips of these filopodia, while APPL1 endosomes accumulate at the base. A combination of MYO6+ mutagenesis and siRNA-mediated depletion of MYO6 binding partners demonstrates that motor activity and binding to endosomal membranes mediated by GIPC and PI(4,5)P2 are crucial for filopodia formation. A similar reorganization of actin is induced by a constitutive dimer of MYO6+, indicating that multimerization of MYO6 on endosomes through binding to GIPC is required for this cellular activity and regulation of actin network structure. This unique engineered MYO6+ offers insights into both filopodia formation and MYO6 motor function at endosomes and at the plasma membrane.

scholarly journals Functional plasticity of polarity proteins controls epithelial tissue architecture

2021 ◽  
Author(s):  
Cornélia Biehler ◽  
Katheryn E. Rothenberg ◽  
Alexandra Jetté ◽  
Hélori-Mael Gaudé ◽  
Rodrigo Fernandez-Gonzalez ◽  
...  
Keyword(s):  
Epithelial Cells ◽  
Domain Size ◽  
Cell Polarization ◽  
Epithelial Tissue ◽  
Tissue Architecture ◽  
Functional Plasticity ◽  
Apical Constriction ◽  
Dynamic Regulation ◽  
Cell Contractility ◽  
Apical Domain

AbstractThe Drosophila polarity protein Crumbs is essential for the establishment and growth of the apical domain in epithelial cells. Dynamic regulation of apical domain size is crucial for forming and maintaining complex epithelial structures such as tubes or acini. The protein Yurt limits the ability of Crumbs to promote apical membrane growth, thereby defining proper apical/basal membrane ratio that is essential for the functional architecture of epithelial cells. Here, we show that Yurt is not a general inhibitor of Crumbs, but rather hijacks Crumbs activity toward specific functions. In particular, Crumbs recruits Yurt to the apical domain to increase Myosin-dependent cortical tension while decreasing relative tissue viscosity. Yurt overexpression thus induces apical constriction in epithelial cells. The kinase aPKC phosphorylates Yurt, thereby dislodging the latter from the apical domain and releasing apical tension. In contrast, the kinase Pak1 promotes Yurt dephosphorylation through activation of the phosphatase PP2A. The Pak1–PP2A module thus opposes aPKC function and supports Yurt-induced apical constriction. Hence, the complex interplay between Yurt, aPKC, Pak1 and PP2A contributes to the functional plasticity of Crumbs. Overall, our data increase our understanding of how proteins sustaining epithelial cell polarization and Myosin-dependent cell contractility interact with one another to control epithelial tissue architecture.

scholarly journals Regions within a single epidermal cell of Drosophila can be planar polarised independently

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Miguel Rovira ◽  
Pedro Saavedra ◽  
José Casal ◽  
Peter A Lawrence
Keyword(s):  
Single Cell ◽  
Larval Development ◽  
Cell Polarity ◽  
Epidermal Cell ◽  
Planar Cell Polarity ◽  
Different Types ◽  
Local Comparison ◽  
Epithelial Sheets

Planar cell polarity (PCP), the coordinated and consistent orientation of cells in the plane of epithelial sheets, is a fundamental and conserved property of animals and plants. Up to now, the smallest unit expressing PCP has been considered to be an entire single cell. We report that, in the larval epidermis of Drosophila, different subdomains of one cell can have opposite polarities. In larvae, PCP is driven by the Dachsous/Fat system; we show that the polarity of a subdomain within one cell is its response to levels of Dachsous/Fat in the membranes of contacting cells. During larval development, cells rearrange (<xref ref-type="bibr" rid="bib25">Saavedra et al., 2014</xref>) and when two subdomains of a single cell have different types of neighbouring cells, then these subdomains can become polarised in opposite directions. We conclude that polarisation depends on a local comparison of the amounts of Dachsous and Fat within opposing regions of a cell's membrane.

scholarly journals Radially-patterned cell behaviours during tube budding from an epithelium

2018 ◽  
Author(s):  
Yara E. Sanchez-Corrales ◽  
Guy B. Blanchard ◽  
Katja Röper
Keyword(s):  
Salivary Gland ◽  
Live Imaging ◽  
Apical Constriction ◽  
Morphogenetic Process ◽  
Early Stages ◽  
Morphometric Methods ◽  
Pit Cells ◽  
Epithelial Sheets

AbstractThe budding of tubular organs from flat epithelial sheets is a vital morphogenetic process. Cell behaviours that drive such processes are only starting to be unraveled. Using live imaging and novel morphometric methods we show that in addition to apical constriction, radially oriented directional intercalation of placodal cells plays a major contribution to the early stages of invagination of the salivary gland tube in the Drosophila embryo. Extending analyses in 3D, we find that near the pit of invagination, isotropic apical constriction leads to strong cell wedging, and further from the pit cells interleave circumferentially, suggesting apically driven behaviours. Supporting this, junctional myosin is enriched in, and neighbour exchanges biased towards the circumferential orientation. In a mutant failing pit specification, neither are biased due to an inactive pit. Thus, tube budding depends on a radially polarised pattern of apical myosin leading to radially oriented 3D cell behaviours, with a close mechanical interplay between invagination and intercalation.

scholarly journals LMO7-dependent apical constriction requires the binding of the Myosin heavy chain

2021 ◽  
Author(s):  
Miho Matsuda ◽  
Chih-Wen Chu ◽  
Sergei S Sokol
Keyword(s):  
Heavy Chain ◽  
Myosin Light Chain ◽  
Myosin Ii ◽  
Tube Formation ◽  
Epithelial Morphogenesis ◽  
Apical Constriction ◽  
Actomyosin Contractility ◽  
Apical Domain ◽  
Underlying Mechanisms ◽  
Muscle Myosin

The reduction of the apical domain, or apical constriction, is a process that occurs in a single cell or is coordinated in a group of cells in the epithelium. Coordinated apical constriction is particularly important when the epithelium is undergoing dynamic morphogenetic events such as furrow or tube formation. However, the underlying mechanisms remain incompletely understood. Here we show that Lim only protein 7 (Lmo7) is a novel activator of apical constriction in the Xenopus superficial ectoderm, which coordinates actomyosin contractility in a group of cells during epithelial morphogenesis. Like other apical constriction regulators, Lmo7 requires the activation of the Rho-Rock-Myosin II pathway to induce apical constriction. However, instead of increasing the phosphorylation of myosin light chain (MLC), Lmo7 binds muscle myosin II heavy chain A (NMIIA) and increases its association with actomyosin bundles at adherens junctions (AJs). Lmo7 overexpression modulates the subcellular distribution of Wtip, a tension marker at AJs, suggesting that Lmo7 generates mechanical forces at AJs. We propose that Lmo7 increases actomyosin contractility at AJs by promoting the formation of actomyosin bundles.

scholarly journals Multifunctional role of GPCR signaling in epithelial tube formation

2022 ◽  
Author(s):  
Vishakha Vishwakarma ◽  
Thao Phuong Le ◽  
SeYeon Chung
Keyword(s):  
Rho Kinase ◽  
Tube Formation ◽  
Dependent Manner ◽  
Cortical Actin ◽  
Apical Constriction ◽  
Gpcr Signaling ◽  
Epithelial Tube ◽  
Cellular Forces ◽  
G Protein Coupled

Epithelial tube formation requires Rho1-dependent actomyosin contractility to generate the cellular forces that drive cell shape changes and rearrangement. Rho1 signaling is activated by G protein-coupled receptor (GPCR) signaling at the cell surface. During Drosophila embryonic salivary gland (SG) invagination, the GPCR ligand Folded gastrulation (Fog) activates Rho1 signaling to drive apical constriction. The SG receptor that transduces the Fog signal into Rho1-dependent myosin activation has not been identified. Here, we reveal that the Smog GPCR transduces Fog signal to regulate Rho kinase accumulation and myosin activation in the apicomedial region of cells to control apical constriction during SG invagination. We also report on unexpected Fog-independent roles for Smog in maintaining epithelial integrity and organizing cortical actin. Our data supports a model wherein Smog regulates distinct myosin pools and actin cytoskeleton in a ligand-dependent manner during epithelial tube formation.

scholarly journals Requirement of Phosphoinositides Containing Stearic Acid To Control Cell Polarity

2015 ◽  
Vol 36 (5) ◽  
pp. 765-780 ◽  
Author(s):  
François Doignon ◽  
Patricia Laquel ◽  
Eric Testet ◽  
Karine Tuphile ◽  
Laetitia Fouillen ◽  
...  
Keyword(s):  
Stearic Acid ◽  
Cell Polarity ◽  
Intracellular Trafficking ◽  
Control Cell ◽  
Cortical Actin ◽  
Content Type ◽  
Cytoskeleton Organization ◽  
Actin Cytoskeleton Organization ◽  
Acyl Chains ◽  
Diploid Cells

Phosphoinositides (PIPs) are present in very small amounts but are essential for cell signaling, morphogenesis, and polarity. By mass spectrometry, we demonstrated that some PIPs with stearic acyl chains were strongly disturbed in apsi1ΔSaccharomyces cerevisiaeyeast strain deficient in the specific incorporation of a stearoyl chain at thesn-1 position of phosphatidylinositol. The absence of PIPs containing stearic acid induced disturbances in intracellular trafficking, although the total amount of PIPs was not diminished. Changes in PIPs also induced alterations in the budding pattern and defects in actin cytoskeleton organization (cables and patches). Moreover, when thePSI1gene was impaired, a high proportion of cells with bipolar cortical actin patches that occurred concomitantly with the bipolar localization of Cdc42p was specifically found among diploid cells. This bipolar cortical actin phenotype, never previously described, was also detected in abud9Δ/bud9Δ strain. Very interestingly, overexpression ofPSI1reversed this phenotype.

Determination of cell polarity in germinated spores and hyphal tips of the filamentous ascomycete Ashbya gossypii requires a rhoGAP homolog

2000 ◽  
Vol 113 (9) ◽  
pp. 1611-1621 ◽  
Author(s):  
J. Wendland ◽  
P. Philippsen
Keyword(s):  
Filamentous Fungi ◽  
Cell Polarity ◽  
Germ Cells ◽  
Rho Gtpases ◽  
Protein Domain ◽  
Ashbya Gossypii ◽  
Cortical Actin ◽  
Filamentous Ascomycete ◽  
Bud Emergence ◽  
Hyphal Tip

In the filamentous ascomycete Ashbya gossypii, like in other filamentous fungi onset of growth in dormant spores occurs as an isotropic growth phase generating spherical germ cells. Thereafter, a switch to polarized growth results in the formation of the first hyphal tip. The initial steps of hyphal tip formation in filamentous fungi, therefore, resemble processes taking place prior to and during bud emergence of unicellular yeast-like fungi. We investigated whether phenotypic similarities between these distinct events extended to the molecular level. To this end we isolated and characterized the A. gossypii homolog of the Saccharomyces cerevisiae BEM2 gene which is part of a network of rho-GTPases and their regulators required for bud emergence and bud growth in yeast. Here we show that the AgBem2 protein contains a GAP- (GTPase activating protein) domain for rho-like GTPases at its carboxy terminus, and that this part of AgBem2p is required for complementation of an Agbem2 null strain. Germination of spores resulted in enlarged Agbem2 germ cells that were unable to generate the bipolar branching pattern found in wild-type germ cells. In addition, mutant hyphae were swollen due to defects in polarized cell growth indicated by the delocalized distribution of chitin and cortical actin patches. Surprisingly, the complete loss of cell polarity which lead to spherical hyphal tips was overcome by the establishment of new cell polarities and the formation of multiple new hyphal tips. In conclusion these results and other findings demonstrate that establishment of cell polarity, maintenance of cell polarity, and polarized hyphal growth in filamentous fungi require members of Ρ-GTPase modules.

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