Membrane remodeling during embryonic abscission in <i>Caenorhabditis elegans</i>

König, Julia; Frankel, Elisa B.; Audhya, Anjon; Müller‐Reichert, Thomas

doi:10.1083/jcb.201607030

Cited by 38 publications

(40 citation statements)

References 54 publications

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“…These assemble sequentially at the limiting membrane of the late endosome (Schuh and Audhya, 2014;Vietri et al, 2019). The ESCRT machinery regulates various cellular processes involved in development (Irion and St Johnston, 2007), neurogenesis (Loncle et al, 2015), virus budding (Carlton et al, 2008), cytokinesis (König et al, 2017;Matias et al, 2015) and autophagy (Lee et al, 2007;Rusten et al, 2007). ESCRT malfunction is also associated with numerous human diseases (for review see Saksena and Emr 2009).…”

Section: Introductionmentioning

confidence: 99%

Accessory ESCRT-III proteins selectively regulate Rab11-exosome biogenesis inDrosophilasecondary cells

Marie

Fan

Mendes

et al. 2020

Preprint

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Exosomes are secreted nanovesicles with potent signalling activity that are initially formed as intraluminal vesicles (ILVs) in multivesicular endosomes, which subsequently fuse with the plasma membrane. These ILVs are made in both late endosomes and recycling endosomes, the latter marked by the small GTPase Rab11 and generating exosomes with different cargos and functions. Core proteins within four Endosomal Sorting Complex Required for Transport (ESCRT) assemblies (0-III) play key sequential roles in late endosomal exosome biogenesis and ILV-mediated destruction of ubiquitinylated cargos through the endolysosomal system. They also control additional cellular processes, such as cytokinesis and other vesicle budding.By contrast, the functions of several accessory ESCRTs are not well defined. Here we assess the ESCRT-dependency of Rab11-exosomes, using RNA knockdown in Drosophila secondary cells (SCs) of the male accessory gland, which have unusually enlarged Rab11-positive compartments. Unexpectedly, not only are core proteins in all four ESCRT complexes required for Rab11-exosome formation, but also accessory ESCRT-III proteins, CHMP1, CHMP5 and IST1. Suppressing expression of these accessory proteins does not affect other aspects of cell morphology, unlike most core ESCRT knockdowns, and does not lead to accumulation of ubiquitinylated cargos. We conclude that accessory ESCRT-III components have a specific and potentially ubiquitin-independent role in Rab11-exosome generation, which might provide a target for blocking the pro-tumorigenic activities of these vesicles in cancer.

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Section: Introductionmentioning

confidence: 99%

Accessory ESCRT-III proteins selectively regulate Rab11-exosome biogenesis inDrosophilasecondary cells

Marie

Fan

Mendes

et al. 2020

Preprint

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“…LEM-2 and CHMP-7 may be involved in constricting NE holes to prevent major NE sealing defects caused by membrane overflow in the absence of CNEP-1. The fact that depletion of chmp-7 in the cnep-1Δ background increases the frequency of internal nuclear membranes after meiosis as well as the percentage of twinned nuclei after mitosis also suggests a potential role for ESCRTs in membrane clearance, which has been proposed as a role for ESCRTs in cytokinetic abscission (König et al, 2017).…”

Section: Resultsmentioning

confidence: 94%

Local regulation of lipid synthesis controls ER sheet insertion into nuclear envelope holes to complete nuclear closure

Penfield

Shankar

Szentgyörgyi

et al. 2019

Preprint

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The nuclear permeability barrier depends on closure of holes in the nuclear envelope (NE). Here, we use meiotic C. elegans oocytes to demonstrate that local control of glycerophospholipid synthesis by CNEP-1/CTDNEP1 regulates the insertion of ER sheets into NE holes and functions independently of ESCRT-III to ensure NE closure.Deletion of CNEP-1 causes excess incorporation of ER membranes into NE holes and a defective NE permeability barrier. ESCRT-III components accumulate at the NE opening surrounding the meiotic spindle, and loss of NE adaptors for ESCRT-III exacerbates NE sealing defects in cnep-1 mutants. Limiting ER sheet production by restoring glycerophospholipid synthesis in cnep-1 mutants rescued NE permeability defects. 3D analysis showed that membrane sheets feed into and narrow NE holes occluded by meiotic spindle microtubules supporting a role for ER sheet insertion in NE closure.Thus, feeding of ER sheets into NE holes must be coordinated with production of ER sheets near the NE to promote NE closure.

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“…9h) 35 . The intercellular bridge no longer permits diffusion between cells ~4 minutes after furrow ingression 34 , but the first cut for abscission does not occur until ~10 minutes after furrow ingression 36 . Therefore, we asked when actomyosin accumulated in the intercellular bridge was accessible for proteasomal degradation.…”

Section: Degron Reporters Reveal Membrane Topology During Abscissionmentioning

confidence: 99%

Degron-tagged reporters probe membrane topology and enable the specific labelling of membrane-wrapped structures

Beer

Fazeli

Irmisch

et al. 2018

Preprint

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Visualization of specific organelles in tissues over background fluorescence can be challenging, especially when reporters localize to multiple structures. Instead of trying to identify proteins enriched in specific membrane-wrapped structures, we used a selective degradation approach to remove reporters from the cytoplasm or nucleus of C. elegans embryos and mammalian cells. We demonstrate specific labelling of organelles using degron-tagged reporters, including extracellular vesicles, as well as individual neighbouring membranes.These degron-tagged reporters facilitate long-term tracking of released cell debris and cell corpses, even during uptake and phagolysosomal degradation. We further show that degron protection assays can probe the topology of the nuclear envelope and plasma membrane during cell division, giving insight into protein and organelle dynamics. As endogenous and heterologous degrons are used in bacteria, yeast, plants, and animals, degron approaches can enable the specific labelling and tracking of proteins, vesicles, organelles, cell fragments, and cells in many model systems.

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Membrane remodeling during embryonic abscission in Caenorhabditis elegans

Cited by 38 publications

References 54 publications

Accessory ESCRT-III proteins selectively regulate Rab11-exosome biogenesis inDrosophilasecondary cells

Accessory ESCRT-III proteins selectively regulate Rab11-exosome biogenesis inDrosophilasecondary cells

Local regulation of lipid synthesis controls ER sheet insertion into nuclear envelope holes to complete nuclear closure

Degron-tagged reporters probe membrane topology and enable the specific labelling of membrane-wrapped structures

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