Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms

Michitaka Masuda, Soichi Takeda, Manami Sone, Takashi Ohki, Hidezo Mori, Yuji Kamioka, Naoki Mochizuki

Research output: Contribution to journalArticle

197 Citations (Scopus)

Abstract

The crescent-shaped BAR (Bin/Amphiphysin/Rvs-homology) domain dimer is a versatile protein module that senses and generates positive membrane curvature. The BAR domain dimer of human endophilin-A1, solved at 3.1 Å, has a unique structure consisting of a pair of helix-loop appendages sprouting out from the crescent. The appendage's short helices form a hydrophobic ridge, which runs across the concave surface at its center. Examining liposome binding and tubulation in vitro using purified BAR domain and its mutants indicated that the ridge penetrates into the membrane bilayer and enhances liposome tubulation. BAR domain-expressing cells exhibited marked plasma membrane tubulation in vivo. Furthermore, a swinging-arm mutant lost liposome tubulation activity yet retaining liposome binding. These data suggested that the rigid crescent dimer shape is crucial for the tubulation. We here propose that the BAR domain drives membrane curvature by coordinate action of the crescent's scaffold mechanism and the ridge's membrane insertion in addition to membrane binding via amino-terminal amphipathic helix.

Original languageEnglish
Pages (from-to)2889-2897
Number of pages9
JournalEMBO Journal
Volume25
Issue number12
DOIs
Publication statusPublished - 2006 Jun 21
Externally publishedYes

Fingerprint

Bins
Liposomes
Membranes
Dimers
Cell membranes
Scaffolds
Cell Membrane
amphiphysin
Proteins

Keywords

  • BAR domain
  • Endophilin
  • Liposome
  • Membrane curvature
  • Membrane insertion

ASJC Scopus subject areas

  • Genetics
  • Cell Biology

Cite this

Masuda, M., Takeda, S., Sone, M., Ohki, T., Mori, H., Kamioka, Y., & Mochizuki, N. (2006). Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. EMBO Journal, 25(12), 2889-2897. https://doi.org/10.1038/sj.emboj.7601176

Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. / Masuda, Michitaka; Takeda, Soichi; Sone, Manami; Ohki, Takashi; Mori, Hidezo; Kamioka, Yuji; Mochizuki, Naoki.

In: EMBO Journal, Vol. 25, No. 12, 21.06.2006, p. 2889-2897.

Research output: Contribution to journalArticle

Masuda, M, Takeda, S, Sone, M, Ohki, T, Mori, H, Kamioka, Y & Mochizuki, N 2006, 'Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms', EMBO Journal, vol. 25, no. 12, pp. 2889-2897. https://doi.org/10.1038/sj.emboj.7601176
Masuda, Michitaka ; Takeda, Soichi ; Sone, Manami ; Ohki, Takashi ; Mori, Hidezo ; Kamioka, Yuji ; Mochizuki, Naoki. / Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms. In: EMBO Journal. 2006 ; Vol. 25, No. 12. pp. 2889-2897.
@article{84159ae69b184f0394f9fe87d6f5dcc4,
title = "Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms",
abstract = "The crescent-shaped BAR (Bin/Amphiphysin/Rvs-homology) domain dimer is a versatile protein module that senses and generates positive membrane curvature. The BAR domain dimer of human endophilin-A1, solved at 3.1 {\AA}, has a unique structure consisting of a pair of helix-loop appendages sprouting out from the crescent. The appendage's short helices form a hydrophobic ridge, which runs across the concave surface at its center. Examining liposome binding and tubulation in vitro using purified BAR domain and its mutants indicated that the ridge penetrates into the membrane bilayer and enhances liposome tubulation. BAR domain-expressing cells exhibited marked plasma membrane tubulation in vivo. Furthermore, a swinging-arm mutant lost liposome tubulation activity yet retaining liposome binding. These data suggested that the rigid crescent dimer shape is crucial for the tubulation. We here propose that the BAR domain drives membrane curvature by coordinate action of the crescent's scaffold mechanism and the ridge's membrane insertion in addition to membrane binding via amino-terminal amphipathic helix.",
keywords = "BAR domain, Endophilin, Liposome, Membrane curvature, Membrane insertion",
author = "Michitaka Masuda and Soichi Takeda and Manami Sone and Takashi Ohki and Hidezo Mori and Yuji Kamioka and Naoki Mochizuki",
year = "2006",
month = "6",
day = "21",
doi = "10.1038/sj.emboj.7601176",
language = "English",
volume = "25",
pages = "2889--2897",
journal = "EMBO Journal",
issn = "0261-4189",
publisher = "Nature Publishing Group",
number = "12",

}

TY - JOUR

T1 - Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms

AU - Masuda, Michitaka

AU - Takeda, Soichi

AU - Sone, Manami

AU - Ohki, Takashi

AU - Mori, Hidezo

AU - Kamioka, Yuji

AU - Mochizuki, Naoki

PY - 2006/6/21

Y1 - 2006/6/21

N2 - The crescent-shaped BAR (Bin/Amphiphysin/Rvs-homology) domain dimer is a versatile protein module that senses and generates positive membrane curvature. The BAR domain dimer of human endophilin-A1, solved at 3.1 Å, has a unique structure consisting of a pair of helix-loop appendages sprouting out from the crescent. The appendage's short helices form a hydrophobic ridge, which runs across the concave surface at its center. Examining liposome binding and tubulation in vitro using purified BAR domain and its mutants indicated that the ridge penetrates into the membrane bilayer and enhances liposome tubulation. BAR domain-expressing cells exhibited marked plasma membrane tubulation in vivo. Furthermore, a swinging-arm mutant lost liposome tubulation activity yet retaining liposome binding. These data suggested that the rigid crescent dimer shape is crucial for the tubulation. We here propose that the BAR domain drives membrane curvature by coordinate action of the crescent's scaffold mechanism and the ridge's membrane insertion in addition to membrane binding via amino-terminal amphipathic helix.

AB - The crescent-shaped BAR (Bin/Amphiphysin/Rvs-homology) domain dimer is a versatile protein module that senses and generates positive membrane curvature. The BAR domain dimer of human endophilin-A1, solved at 3.1 Å, has a unique structure consisting of a pair of helix-loop appendages sprouting out from the crescent. The appendage's short helices form a hydrophobic ridge, which runs across the concave surface at its center. Examining liposome binding and tubulation in vitro using purified BAR domain and its mutants indicated that the ridge penetrates into the membrane bilayer and enhances liposome tubulation. BAR domain-expressing cells exhibited marked plasma membrane tubulation in vivo. Furthermore, a swinging-arm mutant lost liposome tubulation activity yet retaining liposome binding. These data suggested that the rigid crescent dimer shape is crucial for the tubulation. We here propose that the BAR domain drives membrane curvature by coordinate action of the crescent's scaffold mechanism and the ridge's membrane insertion in addition to membrane binding via amino-terminal amphipathic helix.

KW - BAR domain

KW - Endophilin

KW - Liposome

KW - Membrane curvature

KW - Membrane insertion

UR - http://www.scopus.com/inward/record.url?scp=33745559393&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33745559393&partnerID=8YFLogxK

U2 - 10.1038/sj.emboj.7601176

DO - 10.1038/sj.emboj.7601176

M3 - Article

C2 - 16763557

AN - SCOPUS:33745559393

VL - 25

SP - 2889

EP - 2897

JO - EMBO Journal

JF - EMBO Journal

SN - 0261-4189

IS - 12

ER -