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Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes

Protein-mediated membrane remodeling is a ubiquitous and critical process for proper cellular function. Inverse Bin/Amphiphysin/Rvs (I-BAR) domains drive local membrane deformation as a precursor to large-scale membrane remodeling. We employ a multiscale approach to provide the molecular mechanism o...

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Autores principales: Jarin, Zack, Tsai, Feng-Ching, Davtyan, Aram, Pak, Alexander J., Bassereau, Patricia, Voth, Gregory A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Biophysical Society 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697384/
https://www.ncbi.nlm.nih.gov/pubmed/31349990
http://dx.doi.org/10.1016/j.bpj.2019.06.025
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author Jarin, Zack
Tsai, Feng-Ching
Davtyan, Aram
Pak, Alexander J.
Bassereau, Patricia
Voth, Gregory A.
author_facet Jarin, Zack
Tsai, Feng-Ching
Davtyan, Aram
Pak, Alexander J.
Bassereau, Patricia
Voth, Gregory A.
author_sort Jarin, Zack
collection PubMed
description Protein-mediated membrane remodeling is a ubiquitous and critical process for proper cellular function. Inverse Bin/Amphiphysin/Rvs (I-BAR) domains drive local membrane deformation as a precursor to large-scale membrane remodeling. We employ a multiscale approach to provide the molecular mechanism of unusual I-BAR domain-driven membrane remodeling at a low protein surface concentration with near-atomistic detail. We generate a bottom-up coarse-grained model that demonstrates similar membrane-bound I-BAR domain aggregation behavior as our recent Mesoscopic Membrane with Explicit Proteins model. Together, these models bridge several length scales and reveal an aggregation behavior of I-BAR domains. We find that at low surface coverage (i.e., low bound protein density), I-BAR domains form transient, tip-to-tip strings on periodic flat membrane sheets. Inside of lipid bilayer tubules, we find linear aggregates parallel to the axis of the tubule. Finally, we find that I-BAR domains form tip-to-tip aggregates around the edges of membrane domes. These results are supported by in vitro experiments showing low curvature bulges surrounded by I-BAR domains on giant unilamellar vesicles. Overall, our models reveal new I-BAR domain aggregation behavior in membrane tubules and on the surface of vesicles at low surface concentration that add insight into how I-BAR domain proteins may contribute to certain aspects of membrane remodeling in cells.
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spelling pubmed-66973842020-08-06 Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes Jarin, Zack Tsai, Feng-Ching Davtyan, Aram Pak, Alexander J. Bassereau, Patricia Voth, Gregory A. Biophys J Articles Protein-mediated membrane remodeling is a ubiquitous and critical process for proper cellular function. Inverse Bin/Amphiphysin/Rvs (I-BAR) domains drive local membrane deformation as a precursor to large-scale membrane remodeling. We employ a multiscale approach to provide the molecular mechanism of unusual I-BAR domain-driven membrane remodeling at a low protein surface concentration with near-atomistic detail. We generate a bottom-up coarse-grained model that demonstrates similar membrane-bound I-BAR domain aggregation behavior as our recent Mesoscopic Membrane with Explicit Proteins model. Together, these models bridge several length scales and reveal an aggregation behavior of I-BAR domains. We find that at low surface coverage (i.e., low bound protein density), I-BAR domains form transient, tip-to-tip strings on periodic flat membrane sheets. Inside of lipid bilayer tubules, we find linear aggregates parallel to the axis of the tubule. Finally, we find that I-BAR domains form tip-to-tip aggregates around the edges of membrane domes. These results are supported by in vitro experiments showing low curvature bulges surrounded by I-BAR domains on giant unilamellar vesicles. Overall, our models reveal new I-BAR domain aggregation behavior in membrane tubules and on the surface of vesicles at low surface concentration that add insight into how I-BAR domain proteins may contribute to certain aspects of membrane remodeling in cells. The Biophysical Society 2019-08-06 2019-07-02 /pmc/articles/PMC6697384/ /pubmed/31349990 http://dx.doi.org/10.1016/j.bpj.2019.06.025 Text en © 2019 Biophysical Society. http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Articles
Jarin, Zack
Tsai, Feng-Ching
Davtyan, Aram
Pak, Alexander J.
Bassereau, Patricia
Voth, Gregory A.
Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes
title Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes
title_full Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes
title_fullStr Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes
title_full_unstemmed Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes
title_short Unusual Organization of I-BAR Proteins on Tubular and Vesicular Membranes
title_sort unusual organization of i-bar proteins on tubular and vesicular membranes
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697384/
https://www.ncbi.nlm.nih.gov/pubmed/31349990
http://dx.doi.org/10.1016/j.bpj.2019.06.025
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