Literature DB >> 26200865

Regulation of membrane-shape transitions induced by I-BAR domains.

Zhiming Chen1, Zheng Shi1, Tobias Baumgart2.   

Abstract

I-BAR proteins are well-known actin-cytoskeleton adaptors and have been observed to be involved in the formation of plasma membrane protrusions (filopodia). I-BAR proteins contain an all-helical, crescent-shaped IRSp53-MIM domain (IMD) dimer that is believed to be able to couple with a membrane shape. This coupling could involve the sensing and even the generation of negative plasma membrane curvature. Indeed, the in vitro studies have shown that IMDs can induce inward tubulation of liposomes. While N-BAR domains, which generate positive membrane curvature, have received a considerable amount of attention from both theory and experiments, the mechanisms of curvature coupling through IMDs are comparatively less studied and understood. Here we used a membrane-shape stability assay developed recently in our lab to quantitatively characterize IMD-induced membrane-shape transitions. We determined a membrane-shape stability diagram for IMDs that reveals how membrane tension and protein density can comodulate the generation of IMD-induced membrane protrusions. From comparison to analytical theory, we determine three key parameters that characterize the curvature coupling of IMD. We find that the curvature generation capacity of IMDs is significantly stronger compared to that of endophilin, an N-BAR protein known to be involved in plasma membrane shape transitions. Contrary to N-BAR domains, where amphipathic helix insertion is known to promote its membrane curvature generation, for IMDs we find that amphipathic helices inhibit membrane shape transitions, consistent with the inverse curvature that IMDs generate. Importantly, in both of these types of BAR domains, electrostatic interactions affect membrane-binding capacity, but do not appear to affect the curvature generation capacity of the protein. These two types of BAR domain proteins show qualitatively similar membrane shape stability diagrams, suggesting an underlying ubiquitous mechanism by which peripheral proteins regulate membrane curvature.
Copyright © 2015 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2015        PMID: 26200865      PMCID: PMC4621619          DOI: 10.1016/j.bpj.2015.06.010

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  53 in total

1.  Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes.

Authors:  Chen Zhu; Sovan L Das; Tobias Baumgart
Journal:  Biophys J       Date:  2012-04-18       Impact factor: 4.033

Review 2.  How proteins produce cellular membrane curvature.

Authors:  Joshua Zimmerberg; Michael M Kozlov
Journal:  Nat Rev Mol Cell Biol       Date:  2006-01       Impact factor: 94.444

3.  The BAR domain superfamily: membrane-molding macromolecules.

Authors:  Adam Frost; Vinzenz M Unger; Pietro De Camilli
Journal:  Cell       Date:  2009-04-17       Impact factor: 41.582

4.  Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis.

Authors:  Thomas A Masters; Bruno Pontes; Virgile Viasnoff; You Li; Nils C Gauthier
Journal:  Proc Natl Acad Sci U S A       Date:  2013-07-02       Impact factor: 11.205

Review 5.  Molecular force transduction by ion channels: diversity and unifying principles.

Authors:  Sergei Sukharev; Frederick Sachs
Journal:  J Cell Sci       Date:  2012-07-13       Impact factor: 5.285

6.  Theoretical analysis of membrane tension in moving cells.

Authors:  Yonatan Schweitzer; Arnon D Lieber; Kinneret Keren; Michael M Kozlov
Journal:  Biophys J       Date:  2014-01-07       Impact factor: 4.033

Review 7.  Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids.

Authors:  Tobias Baumgart; Benjamin R Capraro; Chen Zhu; Sovan L Das
Journal:  Annu Rev Phys Chem       Date:  2011       Impact factor: 12.703

8.  Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles.

Authors:  N Ben-Tal; B Honig; C Miller; S McLaughlin
Journal:  Biophys J       Date:  1997-10       Impact factor: 4.033

9.  Membrane-induced bundling of actin filaments.

Authors:  Allen P Liu; David L Richmond; Lutz Maibaum; Sander Pronk; Phillip L Geissler; Daniel A Fletcher
Journal:  Nat Phys       Date:  2008-08-31       Impact factor: 20.034

10.  Coordination of membrane and actin cytoskeleton dynamics during filopodia protrusion.

Authors:  Changsong Yang; Matthew Hoelzle; Andrea Disanza; Giorgio Scita; Tatyana Svitkina
Journal:  PLoS One       Date:  2009-05-25       Impact factor: 3.240

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  18 in total

1.  Membrane Shape Instability Induced by Protein Crowding.

Authors:  Zhiming Chen; Ehsan Atefi; Tobias Baumgart
Journal:  Biophys J       Date:  2016-11-01       Impact factor: 4.033

2.  Dynamics of a multicomponent vesicle in shear flow.

Authors:  Kai Liu; Gary R Marple; Jun Allard; Shuwang Li; Shravan Veerapaneni; John Lowengrub
Journal:  Soft Matter       Date:  2017-04-25       Impact factor: 3.679

3.  Simple differences in the protein-membrane attachment mechanism have functional consequences for surface mechanics.

Authors:  K Sapp; L Maibaum; A J Sodt
Journal:  J Chem Phys       Date:  2019-10-28       Impact factor: 3.488

4.  Pulling Membrane Nanotubes from Giant Unilamellar Vesicles.

Authors:  Coline Prévost; Feng-Ching Tsai; Patricia Bassereau; Mijo Simunovic
Journal:  J Vis Exp       Date:  2017-12-07       Impact factor: 1.355

5.  The N-Terminal Amphipathic Helix of Endophilin Does Not Contribute to Its Molecular Curvature Generation Capacity.

Authors:  Zhiming Chen; Chen Zhu; Curtis J Kuo; Jaclyn Robustelli; Tobias Baumgart
Journal:  J Am Chem Soc       Date:  2016-10-28       Impact factor: 15.419

6.  Cations induce shape remodeling of negatively charged phospholipid membranes.

Authors:  Z T Graber; Z Shi; T Baumgart
Journal:  Phys Chem Chem Phys       Date:  2017-06-14       Impact factor: 3.676

Review 7.  Membrane remodeling and mechanics: Experiments and simulations of α-Synuclein.

Authors:  Ana West; Benjamin E Brummel; Anthony R Braun; Elizabeth Rhoades; Jonathan N Sachs
Journal:  Biochim Biophys Acta       Date:  2016-03-10

8.  Suppressing membrane height fluctuations leads to a membrane-mediated interaction among proteins.

Authors:  Kayla Sapp; Lutz Maibaum
Journal:  Phys Rev E       Date:  2016-11-29       Impact factor: 2.529

9.  Opposing Kinesin and Myosin-I Motors Drive Membrane Deformation and Tubulation along Engineered Cytoskeletal Networks.

Authors:  Betsy B McIntosh; Serapion Pyrpassopoulos; Erika L F Holzbaur; E Michael Ostap
Journal:  Curr Biol       Date:  2018-01-11       Impact factor: 10.834

Review 10.  Physical basis of some membrane shaping mechanisms.

Authors:  Mijo Simunovic; Coline Prévost; Andrew Callan-Jones; Patricia Bassereau
Journal:  Philos Trans A Math Phys Eng Sci       Date:  2016-07-28       Impact factor: 4.226

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