WASH phosphorylation balances endosomal versus cortical actin network integrities during epithelial morphogenesis

Tsarouhas, Vasilios; Liú, Dan; Tsikala, Georgia; Fedoseienko, Alina; Zinn, Kai; Matsuda, Ryotaro; Billadeau, Daniel D.; Samakovlis, Christos

doi:10.1038/s41467-019-10229-6

Cited by 24 publications

(27 citation statements)

References 67 publications

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“…This is mediated by Washout (Wash), a Wiskott-Aldrich Syndrome protein family member that activates the Arp2/3 complex thus allowing actin nucleation (Rottner et al, 2017; MacDonald et al, 2018). Wash has been studied in multicellular tubes of the tracheal system, but its role in terminal cell development has not been determined (Dong et al, 2013; Tsarouhas et al, 2019). We found that a UAS-Wash::GFP construct showed a strong, dynamic enrichment around CD4 vesicles (Fig.…”

Section: Resultsmentioning

confidence: 99%

An endosome-associated actin network involved in directed apical plasma membrane growth

Ríos-Barrera

Leptin

2021

Preprint

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The actin cytoskeleton participates in a range of cellular processes. It supports cell shape changes by propagating forces within cells and between cells and their environment. Terminal cells of the Drosophila respiratory system form a subcellular tube by invaginating their apical plasma membrane; cortical actin networks at the basal and apical plasma membranes are critical for proper morphogenesis. Basal actin affects apical membrane morphogenesis, and it is not known how the two separate actin pools communicate. We report here that actin assembles around vesicles of the late endocytic pathway, which are present in the growth cone of the cell, between the tip of the subcellular tube and the leading filopodia of the basal membrane. Actin organized at late endosomes extends towards both membrane compartments. Preventing proper actin nucleation at late endosomes disturbs the directionality of tube growth, uncoupling it from the direction of cell elongation. Severing actin in this area affects tube integrity. These findings demonstrate a role for the late endocytic pathway in organizing actin for proper cell morphogenesis, in addition to its known role in membrane and protein trafficking.

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Section: Resultsmentioning

confidence: 99%

An endosome-associated actin network involved in directed apical plasma membrane growth

Ríos-Barrera

Leptin

2021

Preprint

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“…Another essential process during wound healing is matrix remodeling. Interestingly, WASH was previously implicated in apical endocytosis of extracellular material in the Drosophila airway epithelium during embryogenesis (Tsarouhas et al ., 2019). Hence, WASH-ME could also contribute to matrix remodeling as a specialized mechanism for internalization of extracellular material.…”

Section: Discussionmentioning

confidence: 99%

Endocytic vacuole formation by WASH-mediated endocytosis

Brinkert

Krebs

et al. 2021

Preprint

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Endocytosis of extracellular or plasma membrane material is a fundamental process. A variety of endocytic pathways exist, several of which are barely understood in terms of mechanistic execution and biological function. Importantly, some mechanisms have been identified and characterized by following virus internalization into cells. This includes a novel endocytic pathway exploited by human papillomavirus type 16 (HPV16). However, its cellular role and mechanism of endocytic vacuole formation remain unclear. Here, HPV16 was used as a tool to examine the mechanistic execution of vesicle formation by combining systematic perturbation of cellular processes with electron and video microscopy. Our results indicate cargo uptake by uncoated, inward-budding pits facilitated by the membrane bending retromer protein SNX2. Actin polymerization-driven vesicle scission is promoted by WASH, an actin regulator typically not found at the plasma membrane. Uncovering a novel role of WASH in endocytosis, we propose to term the new pathway WASH-mediated endocytosis (WASH-ME).

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“…The arrangement of the taenidial folds depends primarily on the interaction between endocytosis processes, apical actin formation, and the formation of the chitin-matrix at the apical cell surface. A disturbed taenidial fold arrangement is linked to tube collapse and gas-filling defects 57 – 59 . Our studies suggest that the formation of taenidial chitin requires Cht2.…”

Section: Discussionmentioning

confidence: 99%

Glycosylhydrolase genes control respiratory tubes sizes and airway stability

Behr

Riedel

2020

Sci Rep

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tight barriers are crucial for animals. insect respiratory cells establish barriers through their extracellular matrices. These chitinous-matrices must be soft and flexible to provide ventilation, but also tight enough to allow oxygen flow and protection against dehydration, infections, and environmental stresses. However, genes that control soft, flexible chitin-matrices are poorly known. We investigated the genes of the chitinolytic glycosylhydrolase-family 18 in the tracheal system of Drosophila melanogaster. Our findings show that five chitinases and three chitinase-like genes organize the tracheal chitin-cuticles. Most of the chitinases degrade chitin from airway lumina to enable oxygen delivery. They further improve chitin-cuticles to enhance tube stability and integrity against stresses. Unexpectedly, some chitinases also support chitin assembly to expand the tube lumen properly. Moreover, Chitinase2 plays a decisive role in the chitin-cuticle formation that establishes taenidial folds to support tube stability. Chitinase2 is apically enriched on the surface of tracheal cells, where it controls the chitin-matrix architecture independently of other known cuticular proteins or chitinases. We suppose that the principle mechanisms of chitin-cuticle assembly and degradation require a set of critical glycosylhydrolases for flexible and not-flexible cuticles. The same glycosylhydrolases support thick laminar cuticle formation and are evolutionarily conserved among arthropods. Oxygen uptake is vital for all animals and an essential factor responsible for the limitation of fitness 1. Arthropods, especially insects, actively perform tracheal ventilation and diffusion to oxygenate their organs 2. The tracheal system is a hallmark of insects limiting their sizes, even in terms of giant evolutionary insects when hyperoxia occurred during the late Carboniferous and early Permian 3. The Drosophila respiratory system consists of multicellular and unicellular tubes. They together form a complex airway network that transfers oxygen to target tissues 4,5. Oxygen transport requires barriers to multicellular tracheal tubes. The intercellular diffusion barriers form at the lateral membrane by tight junctions analogous septate junctions (SJs), which prevent the paracellular flow of fluids across the tracheal epithelium into the lumina of the airways 6,7. Chitin-containing cuticles establish extracellular barriers against infections and to withstand tension forces 8,9. These include hydrophobic layers facing the lumen, which are impermeable to in-and outflux of fluids 10. Importantly, tracheal chitin-cuticles assemble to assist tube maturation and partially degrade in subsequent steps to support airway clearance during late embryogenesis 11. A crucial but less understood aspect is how the assembly and degradation of chitin-cuticles can occur 12 while maintaining protective barriers and integrity of the tubular system. Tracheal branching is genetically highly controlled and often evolutionarily conserved 13-17. After initial branc...

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WASH phosphorylation balances endosomal versus cortical actin network integrities during epithelial morphogenesis

Cited by 24 publications

References 67 publications

An endosome-associated actin network involved in directed apical plasma membrane growth

An endosome-associated actin network involved in directed apical plasma membrane growth

Endocytic vacuole formation by WASH-mediated endocytosis

Glycosylhydrolase genes control respiratory tubes sizes and airway stability

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