ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis
The endosomal sorting complexes required for transport (ESCRT) pathway facilitates multiple fundamental membrane remodeling events. Previously, we determined X-ray crystal structures of ESCRT-III subunit Snf7, the yeast CHMP4 ortholog, in its active and polymeric state (Tang et al., 2015). However,...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2016-04-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/15507 |
_version_ | 1818019068045688832 |
---|---|
author | Shaogeng Tang Nicholas J Buchkovich W Mike Henne Sudeep Banjade Yun Jung Kim Scott D Emr |
author_facet | Shaogeng Tang Nicholas J Buchkovich W Mike Henne Sudeep Banjade Yun Jung Kim Scott D Emr |
author_sort | Shaogeng Tang |
collection | DOAJ |
description | The endosomal sorting complexes required for transport (ESCRT) pathway facilitates multiple fundamental membrane remodeling events. Previously, we determined X-ray crystal structures of ESCRT-III subunit Snf7, the yeast CHMP4 ortholog, in its active and polymeric state (Tang et al., 2015). However, how ESCRT-III activation is coordinated by the upstream ESCRT components at endosomes remains unclear. Here, we provide a molecular explanation for the functional divergence of structurally similar ESCRT-III subunits. We characterize novel mutations in ESCRT-III Snf7 that trigger activation, and identify a novel role of Bro1, the yeast ALIX ortholog, in Snf7 assembly. We show that upstream ESCRTs regulate Snf7 activation at both its N-terminal core domain and the C-terminus α6 helix through two parallel ubiquitin-dependent pathways: the ESCRT-I-ESCRT-II-Vps20 pathway and the ESCRT-0-Bro1 pathway. We therefore provide an enhanced understanding for the activation of the spatially unique ESCRT-III-mediated membrane remodeling. |
first_indexed | 2024-04-14T07:47:35Z |
format | Article |
id | doaj.art-fe94cbe0e65e461bbec9cd9f7ae267c1 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-14T07:47:35Z |
publishDate | 2016-04-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
spelling | doaj.art-fe94cbe0e65e461bbec9cd9f7ae267c12022-12-22T02:05:18ZengeLife Sciences Publications LtdeLife2050-084X2016-04-01510.7554/eLife.15507ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesisShaogeng Tang0https://orcid.org/0000-0002-3904-492XNicholas J Buchkovich1W Mike Henne2Sudeep Banjade3Yun Jung Kim4Scott D Emr5https://orcid.org/0000-0002-5408-6781Weill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States; Department of Molecular Biology and Genetics, Cornell University, Ithaca, United StatesWeill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States; Department of Molecular Biology and Genetics, Cornell University, Ithaca, United StatesWeill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States; Department of Molecular Biology and Genetics, Cornell University, Ithaca, United StatesWeill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States; Department of Molecular Biology and Genetics, Cornell University, Ithaca, United StatesWeill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States; Department of Molecular Biology and Genetics, Cornell University, Ithaca, United StatesWeill Institute for Cell and Molecular Biology, Cornell University, Ithaca, United States; Department of Molecular Biology and Genetics, Cornell University, Ithaca, United StatesThe endosomal sorting complexes required for transport (ESCRT) pathway facilitates multiple fundamental membrane remodeling events. Previously, we determined X-ray crystal structures of ESCRT-III subunit Snf7, the yeast CHMP4 ortholog, in its active and polymeric state (Tang et al., 2015). However, how ESCRT-III activation is coordinated by the upstream ESCRT components at endosomes remains unclear. Here, we provide a molecular explanation for the functional divergence of structurally similar ESCRT-III subunits. We characterize novel mutations in ESCRT-III Snf7 that trigger activation, and identify a novel role of Bro1, the yeast ALIX ortholog, in Snf7 assembly. We show that upstream ESCRTs regulate Snf7 activation at both its N-terminal core domain and the C-terminus α6 helix through two parallel ubiquitin-dependent pathways: the ESCRT-I-ESCRT-II-Vps20 pathway and the ESCRT-0-Bro1 pathway. We therefore provide an enhanced understanding for the activation of the spatially unique ESCRT-III-mediated membrane remodeling.https://elifesciences.org/articles/15507ESCRT-IIISnf7activationBro1ESCRT-IESCRT-II |
spellingShingle | Shaogeng Tang Nicholas J Buchkovich W Mike Henne Sudeep Banjade Yun Jung Kim Scott D Emr ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis eLife ESCRT-III Snf7 activation Bro1 ESCRT-I ESCRT-II |
title | ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis |
title_full | ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis |
title_fullStr | ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis |
title_full_unstemmed | ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis |
title_short | ESCRT-III activation by parallel action of ESCRT-I/II and ESCRT-0/Bro1 during MVB biogenesis |
title_sort | escrt iii activation by parallel action of escrt i ii and escrt 0 bro1 during mvb biogenesis |
topic | ESCRT-III Snf7 activation Bro1 ESCRT-I ESCRT-II |
url | https://elifesciences.org/articles/15507 |
work_keys_str_mv | AT shaogengtang escrtiiiactivationbyparallelactionofescrtiiiandescrt0bro1duringmvbbiogenesis AT nicholasjbuchkovich escrtiiiactivationbyparallelactionofescrtiiiandescrt0bro1duringmvbbiogenesis AT wmikehenne escrtiiiactivationbyparallelactionofescrtiiiandescrt0bro1duringmvbbiogenesis AT sudeepbanjade escrtiiiactivationbyparallelactionofescrtiiiandescrt0bro1duringmvbbiogenesis AT yunjungkim escrtiiiactivationbyparallelactionofescrtiiiandescrt0bro1duringmvbbiogenesis AT scottdemr escrtiiiactivationbyparallelactionofescrtiiiandescrt0bro1duringmvbbiogenesis |