Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation

Adell, Manuel Alonso Y; Vogel, Georg F.; Pakdel, Mehrshad; Müller, Martin; Lindner, Herbert; Hess, Michael W.; Teis, David

doi:10.1083/jcb.201310114

Cited by 172 publications

(173 citation statements)

References 66 publications

Supporting

Mentioning

163

Contrasting

Order By: Relevance

“…In contrast, deletions of the yeast ESCRT-III-related subunits cause relatively milder defects in MVB structure, mostly affecting ILV size and luminal membrane surface area (Nickerson et al, 2010). ILVs in yeast MVBs are smaller (mean diameter 24-27 nm; Nickerson et al, 2010;Adell et al, 2014) than those in plants (mean diameter 35-38 nm). However, the variation in ILV sizes due to mutations in LIP5/Vta1p, IST1, and other ESCRT-III accessory subunits shared some similarities.…”

Section: Formation Of Mvb In Plantsmentioning

confidence: 94%

Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development

et al. 2016

View full text Add to dashboard Cite

SKD1 is a core component of the mechanism that degrades plasma membrane proteins via the Endosomal Sorting Complex Required for Transport (ESCRT) pathway. Its ATPase activity and endosomal recruitment are regulated by the ESCRT components LIP5 and IST1. How LIP5 and IST1 affect ESCRT-mediated endosomal trafficking and development in plants is not known. Here we use Arabidopsis mutants to demonstrate that LIP5 controls the constitutive degradation of plasma membrane proteins and the formation of endosomal intraluminal vesicles. Although lip5 mutants were able to polarize the auxin efflux facilitators PIN2 and PIN3, both proteins were mis-sorted to the tonoplast in lip5 root cells. In addition, lip5 root cells over-accumulated PIN2 at the plasma membrane. Consistently with the trafficking defects of PIN proteins, the lip5 roots showed abnormal gravitropism with an enhanced response within the first 4 h after gravistimulation. LIP5 physically interacts with IST1-LIKE1 (ISTL1), a protein predicted to be the Arabidopsis homolog of yeast IST1. However, we found that Arabidopsis contains 12 genes coding for predicted IST1-domain containing proteins (ISTL1-12). Within the ISTL1-6 group, ISTL1 showed the strongest interaction with LIP5, SKD1, and the ESCRT-III-related proteins CHMP1A in yeast two hybrid assays. Through the analysis of single and double mutants, we found that the synthetic interaction of LIP5 with ISTL1, but not with ISTL2, 3, or 6, is essential for normal plant growth, repression of spontaneous cell death, and post-embryonic lethality.

show abstract

Section: Formation Of Mvb In Plantsmentioning

confidence: 94%

Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development

et al. 2016

View full text Add to dashboard Cite

show abstract

“…Disassembly of the ESCRT-III complex is catalyzed by Vps4, an ATPase associated with diverse cellular activities (AAA-ATPase) (20 -24). There is also evidence suggesting that Vps4 directly contributes to membrane fission in some cellular processes (8,20,(25)(26)(27)(28). Because Vps4 is the only energy-consuming enzyme in the ESCRT machinery, it has long been viewed as the master regulator of the system.…”

mentioning

confidence: 99%

“…Binding of the Vps4 MIT domain to the MIM sequences displayed by the membrane-bound ESCRT-III filaments can serve to recruit, assemble, and activate the ATPase (21,25). Beyond the four core ESCRT-III subunits, there exist several proteins whose structural folds are similar to ESCRT-III, including Did2 (CHMP1), Vps60 (CHMP5), and Ist1 (IST1) (17,43).…”

mentioning

confidence: 99%

A Novel Mechanism of Regulating the ATPase VPS4 by Its Cofactor LIP5 and the Endosomal Sorting Complex Required for Transport (ESCRT)-III Protein CHMP5

Vild

Li²,

Guo³

et al. 2015

Journal of Biological Chemistry

View full text Add to dashboard Cite

Background: LIP5 and ESCRT-III are regulators of VPS4 in biological processes that require the ESCRT function. Results: Structural and functional analyses of human VPS4, LIP5, and ESCRT-III interactions are presented. Conclusion: ESCRT-III protein CHMP5 inhibits LIP5-mediated VPS4 activation by inducing a moderate conformational change within LIP5. Significance: This study reveals important mechanistic differences in VPS4 regulation between fungi and metazoans.

show abstract

“…Vps2 also recruits the ATPase associated with a variety of cellular activities (AAA) protein Vps4, the only energy-utilizing ESCRT component (Hanson and Cashikar, 2012;Raiborg and Stenmark, 2009). Active Vps4 forms a hexameric complex that disassembles ESCRT-III, allowing recycling of its components, and also plays an active role in scission of the vesicle neck (Adell et al, 2014;Cashikar et al, 2014;Lata et al, 2008;Monroe et al, 2014;Mueller et al, 2012). In addition to their endocytic functions, ESCRT proteins, including Vps4, are required for cytokinesis, viral budding, protecting viral genomes from degradation, exosome secretion, receptor shedding on microvesicles, assembly of nuclear pore complexes, cholesterol transport and plasma membrane wound repair (Barajas et al, 2014;Choudhuri et al, 2014;Du et al, 2013;de Gassart et al, 2004;Jimenez et al, 2014;Morita, 2012;Nabhan et al, 2012;Tang, 2012;Webster et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Drosophila Vps4 promotes Epidermal growth factor receptor signaling independently of its role in receptor degradation

2015

View full text Add to dashboard Cite

Endocytic trafficking of signaling receptors is an important mechanism for limiting signal duration. Components of the Endosomal Sorting Complexes Required for Transport (ESCRT), which target ubiquitylated receptors to intra-lumenal vesicles (ILVs) of multivesicular bodies, are thought to terminate signaling by the epidermal growth factor receptor (EGFR) and direct it for lysosomal degradation. In a genetic screen for mutations that affect Drosophila eye development, we identified an allele of Vacuolar protein sorting 4 (Vps4), which encodes an AAA ATPase that interacts with the ESCRT-III complex to drive the final step of ILV formation. Photoreceptors are largely absent from Vps4 mutant clones in the eye disc, and even when cell death is genetically prevented, the mutant R8 photoreceptors that develop fail to recruit surrounding cells to differentiate as R1-R7 photoreceptors. This recruitment requires EGFR signaling, suggesting that loss of Vps4 disrupts the EGFR pathway. In imaginal disc cells mutant for Vps4, EGFR and other receptors accumulate in endosomes and EGFR target genes are not expressed; epistasis experiments place the function of Vps4 at the level of the receptor. Surprisingly, Vps4 is required for EGFR signaling even in the absence of Shibire, the Dynamin that internalizes EGFR from the plasma membrane. In ovarian follicle cells, in contrast, Vps4 does not affect EGFR signaling, although it is still essential for receptor degradation. Taken together, these findings indicate that Vps4 can promote EGFR activity through an endocytosis-independent mechanism.

show abstract

Coordinated binding of Vps4 to ESCRT-III drives membrane neck constriction during MVB vesicle formation

Abstract: Vps4 both recycles ESCRT-III subunits and cooperates with ESCRT-III to drive distinct membrane remodeling steps that lead to efficient membrane scission during the biogenesis of multivesicular bodies.

Cited by 172 publications

References 66 publications

Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development

Role of SKD1 Regulators LIP5 and IST1-LIKE1 in Endosomal Sorting and Plant Development

A Novel Mechanism of Regulating the ATPase VPS4 by Its Cofactor LIP5 and the Endosomal Sorting Complex Required for Transport (ESCRT)-III Protein CHMP5

Drosophila Vps4 promotes Epidermal growth factor receptor signaling independently of its role in receptor degradation

Contact Info

Product

Resources

About