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Membrane-Elasticity Model of Coatless Vesicle Budding Induced by ESCRT Complexes (ESCRT-Induced Coatless Vesicle Budding)

The formation of vesicles is essential for many biological processes, in particular for the trafficking of membrane proteins within cells. The Endosomal Sorting Complex Required for Transport (ESCRT) directs membrane budding away from the cytosol. Unlike other vesicle formation pathways, the ESCRT-m... Full description

Journal Title: 2012 Vol.8(10), p.e1002736
Main Author: Różycki, Bartosz
Other Authors: Boura, Evzen , Hurley, James H , Hummer, Gerhard
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: ISSN: 1553-734X ; E-ISSN: 1553-7358 ; DOI: 10.1371/journal.pcbi.1002736
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recordid: plos10.1371/journal.pcbi.1002736
title: Membrane-Elasticity Model of Coatless Vesicle Budding Induced by ESCRT Complexes (ESCRT-Induced Coatless Vesicle Budding)
format: Article
creator:
  • Różycki, Bartosz
  • Boura, Evzen
  • Hurley, James H
  • Hummer, Gerhard
subjects:
  • Research Article
  • Biology
  • Cell Biology
  • Biophysics
ispartof: 2012, Vol.8(10), p.e1002736
description: The formation of vesicles is essential for many biological processes, in particular for the trafficking of membrane proteins within cells. The Endosomal Sorting Complex Required for Transport (ESCRT) directs membrane budding away from the cytosol. Unlike other vesicle formation pathways, the ESCRT-mediated budding occurs without a protein coat. Here, we propose a minimal model of ESCRT-induced vesicle budding. Our model is based on recent experimental observations from direct fluorescence microscopy imaging that show ESCRT proteins colocalized only in the neck region of membrane buds. The model, cast in the framework of membrane elasticity theory, reproduces the experimentally observed vesicle morphologies with physically meaningful parameters. In this parameter range, the minimum energy configurations of the membrane are coatless buds with ESCRTs localized in the bud neck, consistent with experiment. The minimum energy configurations agree with those seen in the fluorescence images, with respect to both bud shapes and ESCRT protein localization. On the basis of our model, we identify distinct mechanistic pathways for the ESCRT-mediated budding process. The bud size is determined by membrane material parameters, explaining the narrow yet different bud size distributions in vitro and in vivo . Our membrane elasticity model thus sheds light on the energetics and possible mechanisms of ESCRT-induced membrane budding. ; Lipid membranes enclose the cytosol of biological cells and compartmentalize their interior. Vesicles are used to transport membrane proteins between cellular compartments. The ESCRT protein machinery induces the creation of such vesicles away from the cytosol. The resulting vesicles are uncoated by protein. Upon vesicle scission and release into the endosome, the ESCRT proteins are recycled into the cytosol. We develop a membrane-elasticity model that captures this budding process. The model reproduces the vesicle morphologies observed in fluorescence microscopy images, and identifies the energetic driving force of vesiculation. We also characterize possible mechanisms of ESCRT-induced membrane budding. The size of the resulting vesicles is determined by membrane material parameters, explaining the narrow yet different bud size distributions and . Our membrane elasticity model thus provides insight into the energetics and mechanisms of uncoated vesicle formation.
language: eng
source:
identifier: ISSN: 1553-734X ; E-ISSN: 1553-7358 ; DOI: 10.1371/journal.pcbi.1002736
fulltext: fulltext
issn:
  • 1553-734X
  • 1553-7358
  • 1553734X
  • 15537358
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titleMembrane-Elasticity Model of Coatless Vesicle Budding Induced by ESCRT Complexes (ESCRT-Induced Coatless Vesicle Budding)
creatorRóżycki, Bartosz ; Boura, Evzen ; Hurley, James H ; Hummer, Gerhard
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descriptionThe formation of vesicles is essential for many biological processes, in particular for the trafficking of membrane proteins within cells. The Endosomal Sorting Complex Required for Transport (ESCRT) directs membrane budding away from the cytosol. Unlike other vesicle formation pathways, the ESCRT-mediated budding occurs without a protein coat. Here, we propose a minimal model of ESCRT-induced vesicle budding. Our model is based on recent experimental observations from direct fluorescence microscopy imaging that show ESCRT proteins colocalized only in the neck region of membrane buds. The model, cast in the framework of membrane elasticity theory, reproduces the experimentally observed vesicle morphologies with physically meaningful parameters. In this parameter range, the minimum energy configurations of the membrane are coatless buds with ESCRTs localized in the bud neck, consistent with experiment. The minimum energy configurations agree with those seen in the fluorescence images, with respect to both bud shapes and ESCRT protein localization. On the basis of our model, we identify distinct mechanistic pathways for the ESCRT-mediated budding process. The bud size is determined by membrane material parameters, explaining the narrow yet different bud size distributions in vitro and in vivo . Our membrane elasticity model thus sheds light on the energetics and possible mechanisms of ESCRT-induced membrane budding. ; Lipid membranes enclose the cytosol of biological cells and compartmentalize their interior. Vesicles are used to transport membrane proteins between cellular compartments. The ESCRT protein machinery induces the creation of such vesicles away from the cytosol. The resulting vesicles are uncoated by protein. Upon vesicle scission and release into the endosome, the ESCRT proteins are recycled into the cytosol. We develop a membrane-elasticity model that captures this budding process. The model reproduces the vesicle morphologies observed in fluorescence microscopy images, and identifies the energetic driving force of vesiculation. We also characterize possible mechanisms of ESCRT-induced membrane budding. The size of the resulting vesicles is determined by membrane material parameters, explaining the narrow yet different bud size distributions and . Our membrane elasticity model thus provides insight into the energetics and mechanisms of uncoated vesicle formation.
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descriptionThe formation of vesicles is essential for many biological processes, in particular for the trafficking of membrane proteins within cells. The Endosomal Sorting Complex Required for Transport (ESCRT) directs membrane budding away from the cytosol. Unlike other vesicle formation pathways, the ESCRT-mediated budding occurs without a protein coat. Here, we propose a minimal model of ESCRT-induced vesicle budding. Our model is based on recent experimental observations from direct fluorescence microscopy imaging that show ESCRT proteins colocalized only in the neck region of membrane buds. The model, cast in the framework of membrane elasticity theory, reproduces the experimentally observed vesicle morphologies with physically meaningful parameters. In this parameter range, the minimum energy configurations of the membrane are coatless buds with ESCRTs localized in the bud neck, consistent with experiment. The minimum energy configurations agree with those seen in the fluorescence images, with respect to both bud shapes and ESCRT protein localization. On the basis of our model, we identify distinct mechanistic pathways for the ESCRT-mediated budding process. The bud size is determined by membrane material parameters, explaining the narrow yet different bud size distributions in vitro and in vivo . Our membrane elasticity model thus sheds light on the energetics and possible mechanisms of ESCRT-induced membrane budding. ; Lipid membranes enclose the cytosol of biological cells and compartmentalize their interior. Vesicles are used to transport membrane proteins between cellular compartments. The ESCRT protein machinery induces the creation of such vesicles away from the cytosol. The resulting vesicles are uncoated by protein. Upon vesicle scission and release into the endosome, the ESCRT proteins are recycled into the cytosol. We develop a membrane-elasticity model that captures this budding process. The model reproduces the vesicle morphologies observed in fluorescence microscopy images, and identifies the energetic driving force of vesiculation. We also characterize possible mechanisms of ESCRT-induced membrane budding. The size of the resulting vesicles is determined by membrane material parameters, explaining the narrow yet different bud size distributions and . Our membrane elasticity model thus provides insight into the energetics and mechanisms of uncoated vesicle formation.
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abstractThe formation of vesicles is essential for many biological processes, in particular for the trafficking of membrane proteins within cells. The Endosomal Sorting Complex Required for Transport (ESCRT) directs membrane budding away from the cytosol. Unlike other vesicle formation pathways, the ESCRT-mediated budding occurs without a protein coat. Here, we propose a minimal model of ESCRT-induced vesicle budding. Our model is based on recent experimental observations from direct fluorescence microscopy imaging that show ESCRT proteins colocalized only in the neck region of membrane buds. The model, cast in the framework of membrane elasticity theory, reproduces the experimentally observed vesicle morphologies with physically meaningful parameters. In this parameter range, the minimum energy configurations of the membrane are coatless buds with ESCRTs localized in the bud neck, consistent with experiment. The minimum energy configurations agree with those seen in the fluorescence images, with respect to both bud shapes and ESCRT protein localization. On the basis of our model, we identify distinct mechanistic pathways for the ESCRT-mediated budding process. The bud size is determined by membrane material parameters, explaining the narrow yet different bud size distributions in vitro and in vivo . Our membrane elasticity model thus sheds light on the energetics and possible mechanisms of ESCRT-induced membrane budding. ; Lipid membranes enclose the cytosol of biological cells and compartmentalize their interior. Vesicles are used to transport membrane proteins between cellular compartments. The ESCRT protein machinery induces the creation of such vesicles away from the cytosol. The resulting vesicles are uncoated by protein. Upon vesicle scission and release into the endosome, the ESCRT proteins are recycled into the cytosol. We develop a membrane-elasticity model that captures this budding process. The model reproduces the vesicle morphologies observed in fluorescence microscopy images, and identifies the energetic driving force of vesiculation. We also characterize possible mechanisms of ESCRT-induced membrane budding. The size of the resulting vesicles is determined by membrane material parameters, explaining the narrow yet different bud size distributions and . Our membrane elasticity model thus provides insight into the energetics and mechanisms of uncoated vesicle formation.
copSan Francisco, USA
pubPublic Library of Science
doi10.1371/journal.pcbi.1002736
oafree_for_read
date2012-10-18