Literature DB >> 26771487

Force Feedback Controls Motor Activity and Mechanical Properties of Self-Assembling Branched Actin Networks.

Peter Bieling1, Tai-De Li2, Julian Weichsel3, Ryan McGorty4, Pamela Jreij5, Bo Huang4, Daniel A Fletcher6, R Dyche Mullins7.   

Abstract

Branched actin networks--created by the Arp2/3 complex, capping protein, and a nucleation promoting factor--generate and transmit forces required for many cellular processes, but their response to force is poorly understood. To address this, we assembled branched actin networks in vitro from purified components and used simultaneous fluorescence and atomic force microscopy to quantify their molecular composition and material properties under various forces. Remarkably, mechanical loading of these self-assembling materials increases their density, power, and efficiency. Microscopically, increased density reflects increased filament number and altered geometry but no change in average length. Macroscopically, increased density enhances network stiffness and resistance to mechanical failure beyond those of isotropic actin networks. These effects endow branched actin networks with memory of their mechanical history that shapes their material properties and motor activity. This work reveals intrinsic force feedback mechanisms by which mechanical resistance makes self-assembling actin networks stiffer, stronger, and more powerful.
Copyright © 2016 Elsevier Inc. All rights reserved.

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Year:  2016        PMID: 26771487      PMCID: PMC5033619          DOI: 10.1016/j.cell.2015.11.057

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


  51 in total

1.  Forces generated during actin-based propulsion: a direct measurement by micromanipulation.

Authors:  Yann Marcy; Jacques Prost; Marie-France Carlier; Cécile Sykes
Journal:  Proc Natl Acad Sci U S A       Date:  2004-04-12       Impact factor: 11.205

2.  Actin branching in the initiation and maintenance of lamellipodia.

Authors:  Marlene Vinzenz; Maria Nemethova; Florian Schur; Jan Mueller; Akihiro Narita; Edit Urban; Christoph Winkler; Christian Schmeiser; Stefan A Koestler; Klemens Rottner; Guenter P Resch; Yuichiro Maeda; J Victor Small
Journal:  J Cell Sci       Date:  2012-03-19       Impact factor: 5.285

Review 3.  Cell mechanics and the cytoskeleton.

Authors:  Daniel A Fletcher; R Dyche Mullins
Journal:  Nature       Date:  2010-01-28       Impact factor: 49.962

Review 4.  Cell mechanics: integrating cell responses to mechanical stimuli.

Authors:  Paul A Janmey; Christopher A McCulloch
Journal:  Annu Rev Biomed Eng       Date:  2007       Impact factor: 9.590

Review 5.  Membrane and actin dynamics interplay at lamellipodia leading edge.

Authors:  Sara Bisi; Andrea Disanza; Chiara Malinverno; Emanuela Frittoli; Andrea Palamidessi; Giorgio Scita
Journal:  Curr Opin Cell Biol       Date:  2013-04-29       Impact factor: 8.382

Review 6.  Bioenergetics and kinetics of microtubule and actin filament assembly-disassembly.

Authors:  T L Hill; M W Kirschner
Journal:  Int Rev Cytol       Date:  1982

7.  How profilin promotes actin filament assembly in the presence of thymosin beta 4.

Authors:  D Pantaloni; M F Carlier
Journal:  Cell       Date:  1993-12-03       Impact factor: 41.582

8.  Reconstructing the orientation distribution of actin filaments in the lamellipodium of migrating keratocytes from electron microscopy tomography data.

Authors:  Julian Weichsel; Edit Urban; J Victor Small; Ulrich S Schwarz
Journal:  Cytometry A       Date:  2012-04-12       Impact factor: 4.355

9.  Direct measurement of the lamellipodial protrusive force in a migrating cell.

Authors:  Marcus Prass; Ken Jacobson; Alex Mogilner; Manfred Radmacher
Journal:  J Cell Biol       Date:  2006-09-11       Impact factor: 10.539

10.  Structural basis of filamin A functions.

Authors:  Fumihiko Nakamura; Teresia M Osborn; Christopher A Hartemink; John H Hartwig; Thomas P Stossel
Journal:  J Cell Biol       Date:  2007-12-03       Impact factor: 10.539

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  85 in total

1.  Registry Kinetics of Myosin Motor Stacks Driven by Mechanical Force-Induced Actin Turnover.

Authors:  Kinjal Dasbiswas; Shiqiong Hu; Alexander D Bershadsky; Samuel A Safran
Journal:  Biophys J       Date:  2019-07-31       Impact factor: 4.033

Review 2.  Function and regulation of the Arp2/3 complex during cell migration in diverse environments.

Authors:  Kristen F Swaney; Rong Li
Journal:  Curr Opin Cell Biol       Date:  2016-05-08       Impact factor: 8.382

3.  Evolutionarily related small viral fusogens hijack distinct but modular actin nucleation pathways to drive cell-cell fusion.

Authors:  Ka Man Carmen Chan; Ashley L Arthur; Johannes Morstein; Meiyan Jin; Abrar Bhat; Dörte Schlesinger; Sungmin Son; Donté A Stevens; David G Drubin; Daniel A Fletcher
Journal:  Proc Natl Acad Sci U S A       Date:  2021-01-05       Impact factor: 11.205

Review 4.  Mechanochemical Signaling Directs Cell-Shape Change.

Authors:  Eric S Schiffhauer; Douglas N Robinson
Journal:  Biophys J       Date:  2017-01-24       Impact factor: 4.033

5.  Design principles for robust vesiculation in clathrin-mediated endocytosis.

Authors:  Julian E Hassinger; George Oster; David G Drubin; Padmini Rangamani
Journal:  Proc Natl Acad Sci U S A       Date:  2017-01-26       Impact factor: 11.205

Review 6.  Theory from the Oster Laboratory Leaps Ahead of Experiment in Understanding Actin-Based Cellular Motility.

Authors:  Thomas D Pollard
Journal:  Biophys J       Date:  2016-10-18       Impact factor: 4.033

Review 7.  Multiscale force sensing in development.

Authors:  Nicoletta I Petridou; Zoltán Spiró; Carl-Philipp Heisenberg
Journal:  Nat Cell Biol       Date:  2017-05-31       Impact factor: 28.824

Review 8.  The Spindle: Integrating Architecture and Mechanics across Scales.

Authors:  Mary Williard Elting; Pooja Suresh; Sophie Dumont
Journal:  Trends Cell Biol       Date:  2018-08-06       Impact factor: 20.808

Review 9.  Balancing forces in migration.

Authors:  Patrick W Oakes
Journal:  Curr Opin Cell Biol       Date:  2018-05-23       Impact factor: 8.382

10.  Force and phosphate release from Arp2/3 complex promote dissociation of actin filament branches.

Authors:  Nandan G Pandit; Wenxiang Cao; Jeffrey Bibeau; Eric M Johnson-Chavarria; Edwin W Taylor; Thomas D Pollard; Enrique M De La Cruz
Journal:  Proc Natl Acad Sci U S A       Date:  2020-05-27       Impact factor: 11.205

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