Literature DB >> 23101629

Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction.

Sandrine Morlot1, Valentina Galli, Marius Klein, Nicolas Chiaruttini, John Manzi, Frédéric Humbert, Luis Dinis, Martin Lenz, Giovanni Cappello, Aurélien Roux.   

Abstract

The GTPase dynamin polymerizes into a helical coat that constricts membrane necks of endocytic pits to promote their fission. However, the dynamin mechanism is still debated because constriction is necessary but not sufficient for fission. Here, we show that fission occurs at the interface between the dynamin coat and the uncoated membrane. At this location, the considerable change in membrane curvature increases the local membrane elastic energy, reducing the energy barrier for fission. Fission kinetics depends on tension, bending rigidity, and the dynamin constriction torque. Indeed, we experimentally find that the fission rate depends on membrane tension in vitro and during endocytosis in vivo. By estimating the energy barrier from the increased elastic energy at the edge of dynamin and measuring the dynamin torque, we show that the mechanical energy spent on dynamin constriction can reduce the energy barrier for fission sufficiently to promote spontaneous fission. :
Copyright © 2012 Elsevier Inc. All rights reserved.

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Year:  2012        PMID: 23101629      PMCID: PMC4290832          DOI: 10.1016/j.cell.2012.09.017

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  40 in total

1.  Stalk model of membrane fusion: solution of energy crisis.

Authors:  Yonathan Kozlovsky; Michael M Kozlov
Journal:  Biophys J       Date:  2002-02       Impact factor: 4.033

2.  Entropy-driven tension and bending elasticity in condensed-fluid membranes.

Authors: 
Journal:  Phys Rev Lett       Date:  1990-04-23       Impact factor: 9.161

3.  Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments.

Authors:  Jan Lipfert; Jacob W J Kerssemakers; Tessa Jager; Nynke H Dekker
Journal:  Nat Methods       Date:  2010-10-17       Impact factor: 28.547

4.  The long and short of membrane fission.

Authors:  Aurélien Roux; Bruno Antonny
Journal:  Cell       Date:  2008-12-26       Impact factor: 41.582

Review 5.  Membrane budding and scission by the ESCRT machinery: it's all in the neck.

Authors:  James H Hurley; Phyllis I Hanson
Journal:  Nat Rev Mol Cell Biol       Date:  2010-06-30       Impact factor: 94.444

6.  Dynamin self-assembles into rings suggesting a mechanism for coated vesicle budding.

Authors:  J E Hinshaw; S L Schmid
Journal:  Nature       Date:  1995-03-09       Impact factor: 49.962

7.  Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins.

Authors:  Benoit Sorre; Andrew Callan-Jones; Jean-Baptiste Manneville; Pierre Nassoy; Jean-François Joanny; Jacques Prost; Bruno Goud; Patricia Bassereau
Journal:  Proc Natl Acad Sci U S A       Date:  2009-03-20       Impact factor: 11.205

8.  A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis.

Authors:  Marcus J Taylor; David Perrais; Christien J Merrifield
Journal:  PLoS Biol       Date:  2011-03-22       Impact factor: 8.029

9.  The secretion-coupled endocytosis correlates with membrane tension changes in RBL 2H3 cells.

Authors:  J Dai; H P Ting-Beall; M P Sheetz
Journal:  J Gen Physiol       Date:  1997-07       Impact factor: 4.086

10.  Computational model of membrane fission catalyzed by ESCRT-III.

Authors:  Gur Fabrikant; Suman Lata; James D Riches; John A G Briggs; Winfried Weissenhorn; Michael M Kozlov
Journal:  PLoS Comput Biol       Date:  2009-11-20       Impact factor: 4.475

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  82 in total

1.  Bending "on the rocks"--a cocktail of biophysical modules to build endocytic pathways.

Authors:  Ludger Johannes; Christian Wunder; Patricia Bassereau
Journal:  Cold Spring Harb Perspect Biol       Date:  2014-01-01       Impact factor: 10.005

Review 2.  Zooming in on the molecular mechanisms of endocytic budding by time-resolved electron microscopy.

Authors:  Fatima-Zahra Idrissi; María Isabel Geli
Journal:  Cell Mol Life Sci       Date:  2013-09-04       Impact factor: 9.261

Review 3.  Building a fission machine--structural insights into dynamin assembly and activation.

Authors:  Joshua S Chappie; Fred Dyda
Journal:  J Cell Sci       Date:  2013-06-18       Impact factor: 5.285

4.  Dynamin triple knockout cells reveal off target effects of commonly used dynamin inhibitors.

Authors:  Ryan J Park; Hongying Shen; Lijuan Liu; Xinran Liu; Shawn M Ferguson; Pietro De Camilli
Journal:  J Cell Sci       Date:  2013-09-17       Impact factor: 5.285

5.  Synthesis of Dynole 34-2, Dynole 2-24 and Dyngo 4a for investigating dynamin GTPase.

Authors:  Mark J Robertson; Fiona M Deane; Phillip J Robinson; Adam McCluskey
Journal:  Nat Protoc       Date:  2014-03-20       Impact factor: 13.491

6.  Feedback regulation between plasma membrane tension and membrane-bending proteins organizes cell polarity during leading edge formation.

Authors:  Kazuya Tsujita; Tadaomi Takenawa; Toshiki Itoh
Journal:  Nat Cell Biol       Date:  2015-05-04       Impact factor: 28.824

7.  The tilted helix model of dynamin oligomers.

Authors:  Avihay Kadosh; Adai Colom; Ben Yellin; Aurélien Roux; Tom Shemesh
Journal:  Proc Natl Acad Sci U S A       Date:  2019-06-12       Impact factor: 11.205

8.  Membrane fission by protein crowding.

Authors:  Wilton T Snead; Carl C Hayden; Avinash K Gadok; Chi Zhao; Eileen M Lafer; Padmini Rangamani; Jeanne C Stachowiak
Journal:  Proc Natl Acad Sci U S A       Date:  2017-04-03       Impact factor: 11.205

Review 9.  The biology of boundary conditions: cellular reconstitution in one, two, and three dimensions.

Authors:  Michael D Vahey; Daniel A Fletcher
Journal:  Curr Opin Cell Biol       Date:  2013-11-12       Impact factor: 8.382

Review 10.  Viral membrane scission.

Authors:  Jeremy S Rossman; Robert A Lamb
Journal:  Annu Rev Cell Dev Biol       Date:  2013-05-31       Impact factor: 13.827

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