Open Access

Cell Reports

, volume 13 , issue 11 , pages 2597-2609

Membrane Charge Directs the Outcome of F-BAR Domain Lipid Binding and Autoregulation

Charlotte Kelley ¹

Emily M Messelaar ¹

Tania L Eskin ¹

Shiyu Wang ¹

Kangkang Song ²

Kalanit Vishnia ³

Agata N. Becalska ¹

Oleg Shupliakov ⁴

Michael M. Hagan ⁵

Dganit Danino ³

Olga S. Sokolova ⁶

Daniela Nicastro ²

A. A. Rodal ¹

Hide authors affiliations Show authors affiliations: 6 affiliations

Rosenstiel Basic Medical Sciences Research Center, Department of Biology, Brandeis University, Waltham, MA 02453, USA. |

Departments of Cell Biology and Biophysics, UT Southwestern Medical Center, Dallas, TX 75390, USA. |

Department of Biotechnology and Food Engineering Technion – Israel Institute of Technology Haifa 32000 (Israel) |

⁴

Department of Neuroscience, Karolinska Institutet, von Eulers väg 3, 171 77 Stockholm, Sweden |

⁵

Martin Fisher School of Physics, Brandeis University, , Waltham, MA 02453, USA. |

⁶

Department of Bioengineering, Faculty of Biology, M.V. Lomonosov Moscow State University, 119991 Moscow, Russia. |

Publication type: Journal Article

Publication date: 2015-12-16

Elsevier

Cell Reports

scimago Q1

wos Q1

SJR: 3.796

CiteScore: 12.9

Impact factor: 6.9

ISSN: 22111247, 26391856

DOI: 10.1016/j.celrep.2015.11.044

Copy DOI

PubMed ID: 26686642

General Biochemistry, Genetics and Molecular Biology

Abstract

F-BAR domain proteins regulate and sense membrane curvature by interacting with negatively charged phospholipids and assembling into higher-order scaffolds. However, regulatory mechanisms controlling these interactions are poorly understood. Here, we show that Drosophila Nervous Wreck (Nwk) is autoregulated by a C-terminal SH3 domain module that interacts directly with its F-BAR domain. Surprisingly, this autoregulation does not mediate a simple "on-off" switch for membrane remodeling. Instead, the isolated Nwk F-BAR domain efficiently assembles into higher-order structures and deforms membranes only within a limited range of negative membrane charge, and autoregulation elevates this range. Thus, autoregulation could either reduce membrane binding or promote higher-order assembly, depending on local cellular membrane composition. Our findings uncover an unexpected mechanism by which lipid composition directs membrane remodeling.

Found

3 citations

Sokolova Olga

DSc in Biological/biomedical sciences, associate professor, professor of the Russian Academy of Sciences

180 publications, 2 606 citations

h-index: 30

Lomonosov Moscow State University

The structure of proteins

Viruses

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GOST |

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GOST Copy

Kelley C. et al. Membrane Charge Directs the Outcome of F-BAR Domain Lipid Binding and Autoregulation // Cell Reports. 2015. Vol. 13. No. 11. pp. 2597-2609.

GOST all authors (up to 50) Copy

Kelley C., Messelaar E. M., Eskin T. L., Wang S., Song K., Vishnia K., Becalska A. N., Shupliakov O., Hagan M. M., Danino D., Sokolova O. S., Nicastro D., Rodal A. A. Membrane Charge Directs the Outcome of F-BAR Domain Lipid Binding and Autoregulation // Cell Reports. 2015. Vol. 13. No. 11. pp. 2597-2609.

RIS |

Cite this

RIS Copy

TY - JOUR

DO - 10.1016/j.celrep.2015.11.044

UR - https://doi.org/10.1016/j.celrep.2015.11.044

TI - Membrane Charge Directs the Outcome of F-BAR Domain Lipid Binding and Autoregulation

T2 - Cell Reports

AU - Kelley, Charlotte

AU - Messelaar, Emily M

AU - Eskin, Tania L

AU - Wang, Shiyu

AU - Song, Kangkang

AU - Vishnia, Kalanit

AU - Becalska, Agata N.

AU - Shupliakov, Oleg

AU - Hagan, Michael M.

AU - Danino, Dganit

AU - Sokolova, Olga S.

AU - Nicastro, Daniela

AU - Rodal, A. A.

PY - 2015

DA - 2015/12/16

PB - Elsevier

SP - 2597-2609

IS - 11

VL - 13

PMID - 26686642

SN - 2211-1247

SN - 2639-1856

ER -

BibTex |

Cite this

BibTex (up to 50 authors) Copy

@article{2015_Kelley,

author = {Charlotte Kelley and Emily M Messelaar and Tania L Eskin and Shiyu Wang and Kangkang Song and Kalanit Vishnia and Agata N. Becalska and Oleg Shupliakov and Michael M. Hagan and Dganit Danino and Olga S. Sokolova and Daniela Nicastro and A. A. Rodal},

title = {Membrane Charge Directs the Outcome of F-BAR Domain Lipid Binding and Autoregulation},

journal = {Cell Reports},

year = {2015},

volume = {13},

publisher = {Elsevier},

month = {dec},

url = {https://doi.org/10.1016/j.celrep.2015.11.044},

number = {11},

pages = {2597--2609},

doi = {10.1016/j.celrep.2015.11.044}

}

MLA

Cite this

MLA Copy

Kelley, Charlotte, et al. “Membrane Charge Directs the Outcome of F-BAR Domain Lipid Binding and Autoregulation.” Cell Reports, vol. 13, no. 11, Dec. 2015, pp. 2597-2609. https://doi.org/10.1016/j.celrep.2015.11.044.

Publisher

Elsevier

Journal

Cell Reports

scimago Q1

wos Q1

SJR

3.796

CiteScore

12.9

Impact factor

6.9

ISSN

22111247 (Print)

26391856 (Print)

Profiles

Olga S Sokolova