ESCRT-mediated vesicle concatenation in plant endosomes

Buono, Rafael Andrade; Leier, André; Páez-Valencia, Julio; Pennington, Janice; Goodman, Kaija; Miller, Nathan D.; Ahlquist, Paul; Marquez‐Lago, Tatiana T.; Otegui, Marisa S.

doi:10.1083/jcb.201612040

Cited by 52 publications

(41 citation statements)

References 58 publications

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“…Importantly, the increased duration of Vps4B at MVEs following EGF stimulation implies that multiple ILVs are likely generated during these extended phases of recruitment. Consistent with this idea, electron tomography of MVEs produced in several systems demonstrates that ILVs are generated repetitively from single endosomal microdomains (24,73). Without the need to reassemble ESCRT machinery de novo for each ILV budding event, the rate at which ubiquitin-modified cargoes are sequestered from the cytoplasm can be accelerated, more rapidly attenuating signal transduction pathways initiated at the cell surface.…”

Section: Discussionmentioning

confidence: 83%

Growth factor stimulation promotes multivesicular endosome biogenesis by prolonging recruitment of the late-acting ESCRT machinery

Quinney

Frankel

Shankar

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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The formation of multivesicular endosomes (MVEs) mediates the turnover of numerous integral membrane proteins and has been implicated in the down-regulation of growth factor signaling, thereby exhibiting properties of a tumor suppressor. The endosomal sorting complex required for transport (ESCRT) machinery plays a key role in MVE biogenesis, enabling cargo selection and intralumenal vesicle (ILV) budding. However, the spatiotemporal pattern of endogenous ESCRT complex assembly and disassembly in mammalian cells remains poorly defined. By combining CRISPR/Cas9-mediated genome editing and live cell imaging using lattice light sheet microscopy (LLSM), we determined the native dynamics of both early-and late-acting ESCRT components at MVEs under multiple growth conditions. Specifically, our data indicate that ESCRT-0 accumulates quickly on endosomes, typically in less than 30 seconds, and its levels oscillate in a manner dependent on the downstream recruitment of ESCRT-I. Similarly, levels of the ESCRT-I complex also fluctuate on endosomes, but its average residency time is more than fivefold shorter compared with ESCRT-0. Vps4 accumulation is the most transient, however, suggesting that the completion of ILV formation occurs rapidly. Upon addition of epidermal growth factor (EGF), both ESCRT-I and Vps4 are retained at endosomes for dramatically extended periods of time, while ESCRT-0 dynamics are only modestly affected. Our findings are consistent with a model in which growth factor stimulation stabilizes late-acting components of the ESCRT machinery at endosomes to accelerate the rate of ILV biogenesis and attenuate signal transduction initiated by receptor activation. lattice light sheet microscopy | ESCRT microdomain | CRISPR/Cas9 | epidermal growth factor receptor | organelle

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Section: Discussionmentioning

confidence: 83%

Growth factor stimulation promotes multivesicular endosome biogenesis by prolonging recruitment of the late-acting ESCRT machinery

Quinney

Frankel

Shankar

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, in contrast to what is found in yeast, mutants defective in the ESCRT-pathway in Arabidopsis do not typically accumulate stacked membranes called class-E compartments but rather show clustered or enlarged MVEs (Haas et al, 2007;Kalinowska et al, 2015). Plant MVEs, upon closer ultrastructural examination, do not show typical ILVs, but often generate concatenated vesicles (Buono et al, 2017). Thus, studying the regulation of endocytosis and membrane trafficking in plants not only gives insights into the evolutional flexibility of this pathway, but could also reveal insights into the molecular mechanisms of endocytic trafficking processes in other species.…”

Section: Discussionmentioning

confidence: 87%

Ubiquitin recognition in endocytic trafficking – with or without ESCRT-0

Mosesso

Nagel

Isono

2019

Journal of Cell Science

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The ability to sense and adapt to the constantly changing environment is important for all organisms. Cell surface receptors and transporters are key for the fast response to extracellular stimuli and, thus, their abundance on the plasma membrane has to be strictly controlled. Heteromeric endosomal sorting complexes required for transport (ESCRTs) are responsible for mediating the post-translational degradation of endocytosed plasma membrane proteins in eukaryotes and are essential both in animals and plants. ESCRTs bind and sort ubiquitylated cargoes for vacuolar degradation. Although many components that comprise the multi-subunit ESCRT-0, ESCRT-I, ESCRT-II and ESCRT-III complexes are conserved in eukaryotes, plant and animal ESCRTs have diverged during the course of evolution. Homologues of ESCRT-0, which recognises ubiquitylated cargo, have emerged in metazoan and fungi but are not found in plants. Instead, the Arabidopsis genome encodes plant-specific ubiquitin adaptors and a greater number of target of Myb protein 1 (TOM1) homologues than in mammals. In this Review, we summarise and discuss recent findings on ubiquitin-binding proteins in Arabidopsis that could have equivalent functions to ESCRT-0. We further hypothesise that SH3 domain-containing proteins might serve as membrane curvature-sensing endophilin and amphiphysin homologues during plant endocytosis.

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“…Indeed, in the more artificial scenarios that we present here, be it at sites of chm7OPEN accumulation or Chm7 in vps4Δ cells (Figures 6 and 7), there are obvious parallels between the morphologies observed at the INM and those at the plasma membrane (von Schwedler et al, 2003;Hanson et al, 2008;Morita et al, 2011;Cashikar et al, 2014;Jackson et al, 2017), and at endosomes (Adell et al, 2014;Wenzel et al, 2018) in the context of mutants that stall or inhibit membrane scission. They also resemble more physiological circumstances like in the ILVs of A. thaliana (Buono et al, 2017) and C. elegans (Frankel et al, 2017), which resemble beads on a string. The network of INM evaginations also resemble the fenestrated membrane cisternae formed in the ERderived unconventional secretion pathway, CUPS (Curwin et al, 2016).…”

Section: Discussionmentioning

confidence: 98%

An ESCRT-LEM domain inner nuclear membrane protein surveillance system is poised to directly monitor the integrity of the nuclear envelope barrier and nuclear transport system

Thaller

Allegretti²,

Borah

et al. 2019

Preprint

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The integrity of the nuclear envelope membranes coupled to the diffusion barrier and selective transport properties of nuclear pore complexes (NPCs) are a prerequisite for the robust segregation of nucleoplasm and cytoplasm. Recent work supports that mechanical membrane disruption or perturbation to NPC assembly can trigger an ESCRT-dependent surveillance system that seals nuclear envelope pores: how these pores are sensed and sealed remains to be fully defined. Here, we show that the principal components of the nuclear envelope surveillance system in yeast, which includes the ESCRT Chm7 and the integral inner nuclear membrane (INM) protein Heh1, are spatially segregated by the nuclear transport system. Specifically, at steady state Chm7 is actively restricted from the nucleus by Crm1/Xpo1. Consistent with the idea that it is the exposure of the INM that triggers surveillance, the expression of a transmembrane anchor and the winged helix domain of Heh1 is sufficient to recruit and activate Chm7 at a membrane interface. Correlative light electron tomography under conditions of Chm7 hyper-activation further show the formation of an elaborate network of fenestrated sheets at the INM and suggest ER-membrane delivery at sites of nuclear envelope herniation. Our data point to a model in which exposure of Chm7 to Heh1, driven by any perturbation in the nuclear envelope barrier would lead to local nuclear envelope remodeling to promote membrane sealing. Our findings have implications for disease mechanisms associated with defects in NPC assembly and nuclear envelope integrity.* *

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ESCRT-mediated vesicle concatenation in plant endosomes

Cited by 52 publications

References 58 publications

Growth factor stimulation promotes multivesicular endosome biogenesis by prolonging recruitment of the late-acting ESCRT machinery

Growth factor stimulation promotes multivesicular endosome biogenesis by prolonging recruitment of the late-acting ESCRT machinery

Ubiquitin recognition in endocytic trafficking – with or without ESCRT-0

An ESCRT-LEM domain inner nuclear membrane protein surveillance system is poised to directly monitor the integrity of the nuclear envelope barrier and nuclear transport system

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