In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension

Summary: Artificial cells can shed new light on the molecular basis for life and hold potential for new chemical technologies. Inspired by how nature dynamically regulates its membrane compartments, we aim to repurpose the endosomal sorting complex required for transport (ESCRT) to generate complex...

Full description

Bibliographic Details
Main Authors: Andrew Booth, Christopher J. Marklew, Barbara Ciani, Paul A. Beales
Format: Article
Language:English
Published: Elsevier 2019-05-01
Series:iScience
Online Access:http://www.sciencedirect.com/science/article/pii/S258900421930118X
_version_ 1811282112532185088
author Andrew Booth
Christopher J. Marklew
Barbara Ciani
Paul A. Beales
author_facet Andrew Booth
Christopher J. Marklew
Barbara Ciani
Paul A. Beales
author_sort Andrew Booth
collection DOAJ
description Summary: Artificial cells can shed new light on the molecular basis for life and hold potential for new chemical technologies. Inspired by how nature dynamically regulates its membrane compartments, we aim to repurpose the endosomal sorting complex required for transport (ESCRT) to generate complex membrane architectures as suitable scaffolds for artificial cells. Purified ESCRT-III components perform topological transformations on giant unilamellar vesicles to create complex “vesicles-within-a-vesicle” architectures resembling the compartmentalization in eukaryotic cells. Thus far, the proposed mechanisms for this activity are based on how assembly and disassembly of ESCRT-III on the membrane drives deformation. Here we demonstrate the existence of a negative feedback mechanism from membrane mechanics that regulates ESCRT-III remodeling activity. Intraluminal vesicle (ILV) formation removes excess membrane area, increasing tension, which in turn suppresses downstream ILV formation. This mechanism for in vitro regulation of ESCRT-III activity may also have important implications for its in vivo functions. : Biochemistry; Bioengineering; Cell Biology; Biophysics Subject Areas: Biochemistry, Bioengineering, Cell Biology, Biophysics
first_indexed 2024-04-13T01:45:46Z
format Article
id doaj.art-e264cc031f0d49cb8cde9be9055b535b
institution Directory Open Access Journal
issn 2589-0042
language English
last_indexed 2024-04-13T01:45:46Z
publishDate 2019-05-01
publisher Elsevier
record_format Article
series iScience
spelling doaj.art-e264cc031f0d49cb8cde9be9055b535b2022-12-22T03:08:02ZengElsevieriScience2589-00422019-05-0115173184In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane TensionAndrew Booth0Christopher J. Marklew1Barbara Ciani2Paul A. Beales3School of Chemistry and Astbury Centre for Structural Molecular Biology, University of Leeds, Leeds LS2 9JT, UKDepartment of Chemistry and Centre for Membrane Interactions and Dynamics, University of Sheffield, Sheffield S3 7HF, UKDepartment of Chemistry and Centre for Membrane Interactions and Dynamics, University of Sheffield, Sheffield S3 7HF, UK; Corresponding authorSchool of Chemistry and Astbury Centre for Structural Molecular Biology, University of Leeds, Leeds LS2 9JT, UK; Corresponding authorSummary: Artificial cells can shed new light on the molecular basis for life and hold potential for new chemical technologies. Inspired by how nature dynamically regulates its membrane compartments, we aim to repurpose the endosomal sorting complex required for transport (ESCRT) to generate complex membrane architectures as suitable scaffolds for artificial cells. Purified ESCRT-III components perform topological transformations on giant unilamellar vesicles to create complex “vesicles-within-a-vesicle” architectures resembling the compartmentalization in eukaryotic cells. Thus far, the proposed mechanisms for this activity are based on how assembly and disassembly of ESCRT-III on the membrane drives deformation. Here we demonstrate the existence of a negative feedback mechanism from membrane mechanics that regulates ESCRT-III remodeling activity. Intraluminal vesicle (ILV) formation removes excess membrane area, increasing tension, which in turn suppresses downstream ILV formation. This mechanism for in vitro regulation of ESCRT-III activity may also have important implications for its in vivo functions. : Biochemistry; Bioengineering; Cell Biology; Biophysics Subject Areas: Biochemistry, Bioengineering, Cell Biology, Biophysicshttp://www.sciencedirect.com/science/article/pii/S258900421930118X
spellingShingle Andrew Booth
Christopher J. Marklew
Barbara Ciani
Paul A. Beales
In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension
iScience
title In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension
title_full In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension
title_fullStr In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension
title_full_unstemmed In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension
title_short In Vitro Membrane Remodeling by ESCRT is Regulated by Negative Feedback from Membrane Tension
title_sort in vitro membrane remodeling by escrt is regulated by negative feedback from membrane tension
url http://www.sciencedirect.com/science/article/pii/S258900421930118X
work_keys_str_mv AT andrewbooth invitromembraneremodelingbyescrtisregulatedbynegativefeedbackfrommembranetension
AT christopherjmarklew invitromembraneremodelingbyescrtisregulatedbynegativefeedbackfrommembranetension
AT barbaraciani invitromembraneremodelingbyescrtisregulatedbynegativefeedbackfrommembranetension
AT paulabeales invitromembraneremodelingbyescrtisregulatedbynegativefeedbackfrommembranetension