Formation of membrane ridges and scallops by the F-BAR protein nervous wreck

Agata N. Becalska, Charlotte F. Kelley, Cristina Berciu, Tatiana B. Stanishneva-Konovalova, Xiaofeng Fu, ShiYu Wang, Olga S. Sokolova, Daniela Nicastro, Avital A. Rodal

Research output: Contribution to journalArticle

23 Scopus citations

Abstract

Eukaryotic cells are defined by extensive intracellular compartmentalization, which requires dynamic membrane remodeling. FER/Cip4 homology-Bin/amphiphysin/Rvs (F-BAR) domain family proteins form crescent-shaped dimers, which can bend membranes into buds and tubules of defined geometry and lipid composition. However, these proteins exhibit an unexplained wide diversity of membrane-deforming activities in vitro and functions in vivo. We find that the F-BAR domain of the neuronal protein Nervous Wreck (Nwk) has a novel higher-order structure and membrane-deforming activity that distinguishes it from previously described F-BAR proteins. The Nwk F-BAR domain assembles into zigzags, creating ridges and periodic scallops on membranes in vitro. This activity depends on structural determinants at the tips of the F-BAR dimer and on electrostatic interactions of the membrane with the F-BAR concave surface. In cells, Nwk-induced scallops can be extended by cytoskeletal forces to produce protrusions at the plasma membrane. Our results define a new F-BAR membrane-deforming activity and illustrate a molecular mechanism by which positively curved F-BAR domains can produce a variety of membrane curvatures. These findings expand the repertoire of F-BAR domain mediated membrane deformation and suggest that unique modes of higher-order assembly can define how these proteins sculpt the membrane.

Original languageEnglish (US)
Pages (from-to)2406-2418
Number of pages13
JournalMolecular biology of the cell
Volume24
Issue number15
DOIs
StatePublished - Aug 1 2013

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

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    Becalska, A. N., Kelley, C. F., Berciu, C., Stanishneva-Konovalova, T. B., Fu, X., Wang, S., Sokolova, O. S., Nicastro, D., & Rodal, A. A. (2013). Formation of membrane ridges and scallops by the F-BAR protein nervous wreck. Molecular biology of the cell, 24(15), 2406-2418. https://doi.org/10.1091/mbc.E13-05-0271