The actin regulators Enabled and Diaphanous direct distinct protrusive behaviors in different tissues during<i>Drosophila</i>development

Nowotarski, Stephanie H.; McKeon, Natalie; Moser, Rachel J.; Peifer, Mark

doi:10.1091/mbc.e14-05-0951

Cited by 39 publications

(40 citation statements)

References 93 publications

(133 reference statements)

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“…We also noted that the plane of the zipping canthi was typically deeper than the rest of the LE (Fig. 2E,F), a pattern observed in other mutants (Nowotarski et al, 2014) but of unknown cause. Finally, cell adhesion between the AS and epidermis was typically maintained as closure proceeded, although in some specimens the LE pursestring was less uniform and tissues detached as final segments approached the midline, presumably yielding those cuticles with a hole or scab.…”

Section: Pvr Protein Expression In the As And Ectodermsupporting

confidence: 68%

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

et al. 2015

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A leading cause of human birth defects is the incomplete fusion of tissues, often manifested in the palate, heart, or neural tube. To investigate the molecular control of tissue fusion, embryonic dorsal closure and pupal thorax closure in Drosophila are useful experimental models. We find that Pvr mutants have defects in dorsal midline closure with incomplete amnioserosa internalization and epidermal zippering, as well as cardia bifida. These defects are relatively mild in comparison to those seen with other signaling mutants such as the JNK pathway, and we demonstrate that JNK signaling is not perturbed by altering Pvr receptor tyrosine kinase activity. Rather, modulation of Pvr levels in the ectoderm has an impact on PIP3 membrane accumulation consistent with a link to PI3K signal transduction. Polarized PI3K activity influences protrusive activity from the epidermal leading edge and protrusion area changes in accord with Pvr signaling intensity, providing a possible mechanism to explain Pvr mutant phenotypes. Tissue specific rescue experiments indicate a partial requirement in epithelial tissue, but confirm the essential role of Pvr in the hemocytes for embryonic survival. Taken together, we argue that inefficient removal of the internalizing amnioserosa tissue by mutant hemocytes coupled with impaired midline zippering of mutant epithelium creates a situation in some embryos where dorsal midline closure is incomplete. Based on these observations, we suggest that efferocytosis (corpse clearance) could contribute to proper tissue closure and thus may underlie some congenital birth defects.

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Section: Pvr Protein Expression In the As And Ectodermsupporting

confidence: 68%

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

et al. 2015

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“…3F ( Kaltschmidt et al, 2002), reminiscent of its enrichment at tricellular junctions earlier in embryogenesis (Sawyer et al, 2009;Bonello et al, 2018). In our earlier work we also identified a distinctive localization for the actin polymerization regulator Enabled (Ena) at these special tricellular junctions (Gates et al, 2007;Choi et al, 2011;Nowotarski et al, 2014). In vitro, Ena localizes to growing (barbed) ends of actin filaments (reviewed in Edwards et al, 2014) Ena is required for effective cell shape change during dorsal closure (Gates et al, 2007).…”

Section: Canoe Is Required To Maintain Homeostatic Cell Shapes and Bamentioning

confidence: 96%

The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

Manning

Perez-Vale

Schaefer

et al. 2019

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During morphogenesis cells must change shape and move without disrupting tissue integrity. This requires cell-cell junctions to allow dynamic remodeling while resisting force generated by the actomyosin cytoskeleton. Multiple proteins play roles in junctional-cytoskeletal linkage, but the mechanisms by which they act remain unclear. Drosophila Canoe maintains adherens junction-cytoskeletal linkage during gastrulation.Canoe's mammalian homolog Afadin plays similar roles in cultured cells, working in parallel with ZO-1 proteins, particularly at multicellular junctions. We took these insights back into the fly embryo, exploring how cells maintain epithelial integrity when challenged by adherens junction remodeling during germband extension and dorsal closure. We found Canoe helps cells maintain junctional-cytoskeletal linkage when challenged by the junctional remodeling inherent in mitosis, cell intercalation and neuroblast invagination, or by forces generated by the actomyosin cable at the leading edge. However, even in the absence of Canoe many cells retain epithelial integrity. This is explained by a parallel role played by the ZO-1 homolog Polychaetoid. In embryos lacking both Canoe and Polychaetoid, cell junctions fail early, with multicellular junctions especially sensitive, leading to widespread loss of epithelial integrity. Our data suggest Canoe and Polychaetoid stabilize Bazooka/Par3 at cell-cell junctions, helping maintain balanced apical contractility and tissue integrity.

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“…Yet, it is increasingly clear that membrane reservoirs, in the form of cell surface pits and protrusions, can also take up excess membrane to shrink cell surfaces, and release membrane to fuel cell surface growth (Clark et al, 2014; Figard and Sokac, 2014). For example, as apparent cell surface area gets smaller during apical cell constriction in gastrulating embryos, or during oscillatory contractions in cultured cells, membrane reservoirs of blebs, folds, and filopodia form (Kapustina et al, 2013; Martin et al, 2010; Nowotarski et al, 2014; Sweeton et al, 1991). Conversely, to prevent plasma membrane rupture during mechanical stretching in human myotubes and endothelial cells, reservoirs of surface invaginations flatten out (Cheng et al, 2015; Sinha et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir

et al. 2016

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Cells store membrane in surface reservoirs of pits and protrusions. These membrane reservoirs facilitate cell shape change and buffer mechanical stress; but we do not know how reservoir dynamics are regulated. During cellularization, the first cytokinesis in Drosophila embryos, a reservoir of microvilli unfolds to fuel cleavage furrow ingression. We find that regulated exocytosis adds membrane to the reservoir before and during unfolding. Dynamic F-actin deforms exocytosed membrane into microvilli. Single microvilli extend and retract in ~20 seconds, while the overall reservoir is depleted in sync with furrow ingression over 60–70 minutes. Using pharmacological and genetic perturbations, we show that exocytosis promotes microvillar F-actin assembly, while furrow ingression controls microvillar F-actin disassembly. Thus, reservoir F-actin and, consequently, reservoir dynamics are regulated by membrane supply from exocytosis and membrane demand from furrow ingression.

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The actin regulators Enabled and Diaphanous direct distinct protrusive behaviors in different tissues duringDrosophiladevelopment

Cited by 39 publications

References 93 publications

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

Pvr receptor tyrosine kinase promotes tissue closure by coordinating corpse removal and epidermal zippering

The Drosophila Afadin and ZO-1 homologs Canoe and Polychaetoid act in parallel to maintain epithelial integrity when challenged by adherens junction remodeling

Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir

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