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Membrane-elasticity model of Coatless vesicle budding induced by ESCRT complexes.

Różycki B, Boura E, Hurley JH, Hummer G - PLoS Comput. Biol. (2012)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, USA.

ABSTRACT
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.

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Relation between energetic and geometric properties, obtained by numerical minimization of the energy functional Eq. (6) for fixed parameters  and .(A) Minimum energy  rescaled by the membrane bending rigidity  as a function of the ESCRT binding energy  rescaled by the area  of the lipid-segregated domain. (B) Minimum energy  as a function of the cosine of the membrane tangent angle  along the lines of longitude at the boundary of the ESCRT-coated domain. (C)  as a function of the binding energy  rescaled by the area  of the lipid-segregated domain . (D)  as a function of the area fraction , where  is the area of the ESCRT-rich domain .
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pcbi-1002736-g003: Relation between energetic and geometric properties, obtained by numerical minimization of the energy functional Eq. (6) for fixed parameters and .(A) Minimum energy rescaled by the membrane bending rigidity as a function of the ESCRT binding energy rescaled by the area of the lipid-segregated domain. (B) Minimum energy as a function of the cosine of the membrane tangent angle along the lines of longitude at the boundary of the ESCRT-coated domain. (C) as a function of the binding energy rescaled by the area of the lipid-segregated domain . (D) as a function of the area fraction , where is the area of the ESCRT-rich domain .

Mentions: The spherical cap model predicts discontinuous transitions between the different morphological phases, with a kink in the minimum energy at the transition lines. In the complete model, however, the kink is rounded at the transition line due to the finite-size of the bud neck (Fig. 3A).


Membrane-elasticity model of Coatless vesicle budding induced by ESCRT complexes.

Różycki B, Boura E, Hurley JH, Hummer G - PLoS Comput. Biol. (2012)

Relation between energetic and geometric properties, obtained by numerical minimization of the energy functional Eq. (6) for fixed parameters  and .(A) Minimum energy  rescaled by the membrane bending rigidity  as a function of the ESCRT binding energy  rescaled by the area  of the lipid-segregated domain. (B) Minimum energy  as a function of the cosine of the membrane tangent angle  along the lines of longitude at the boundary of the ESCRT-coated domain. (C)  as a function of the binding energy  rescaled by the area  of the lipid-segregated domain . (D)  as a function of the area fraction , where  is the area of the ESCRT-rich domain .
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3475702&req=5

pcbi-1002736-g003: Relation between energetic and geometric properties, obtained by numerical minimization of the energy functional Eq. (6) for fixed parameters and .(A) Minimum energy rescaled by the membrane bending rigidity as a function of the ESCRT binding energy rescaled by the area of the lipid-segregated domain. (B) Minimum energy as a function of the cosine of the membrane tangent angle along the lines of longitude at the boundary of the ESCRT-coated domain. (C) as a function of the binding energy rescaled by the area of the lipid-segregated domain . (D) as a function of the area fraction , where is the area of the ESCRT-rich domain .
Mentions: The spherical cap model predicts discontinuous transitions between the different morphological phases, with a kink in the minimum energy at the transition lines. In the complete model, however, the kink is rounded at the transition line due to the finite-size of the bud neck (Fig. 3A).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Chemical Physics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, USA.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus