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

Peter Bieling; Tai-De Li; Julian Weichsel; Ryan McGorty; Pamela Jreij; Bo Huang; Daniel A Fletcher; R Dyche Mullins

doi:10.1016/j.cell.2015.11.057

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

Cell. 2016 Jan 14;164(1-2):115-127. doi: 10.1016/j.cell.2015.11.057.

Authors

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

Affiliations

¹ Department of Cellular and Molecular Pharmacology and Howard Hughes Medical Institute, University of California, San Francisco, Genentech Hall, 600 16(th) Street, San Francisco, CA 94158, USA; Department of Bioengineering and Biophysics Program, University of California, Berkeley, 648 Stanley Hall MC 1762, Berkeley, CA 94720, USA.
² Department of Bioengineering and Biophysics Program, University of California, Berkeley, 648 Stanley Hall MC 1762, Berkeley, CA 94720, USA; Physical Biosciences Division, Lawrence Berkeley National Laboratory, 648 Stanley Hall MC 1762, Berkeley, CA 94720, USA; Advance Science Research Center, City University of New York, 85 St. Nicholas Terrace, New York, NY 10031, USA.
³ Department of Chemistry, University of California, Berkeley, 207 Gilman Hall, Berkeley, CA 94720, USA.
⁴ Department of Biochemistry and Biophysics, University of California, San Francisco, Genentech Hall, 600 16(th) Street, San Francisco, CA 94158, USA.
⁵ Department of Bioengineering and Biophysics Program, University of California, Berkeley, 648 Stanley Hall MC 1762, Berkeley, CA 94720, USA.
⁶ Department of Bioengineering and Biophysics Program, University of California, Berkeley, 648 Stanley Hall MC 1762, Berkeley, CA 94720, USA; Physical Biosciences Division, Lawrence Berkeley National Laboratory, 648 Stanley Hall MC 1762, Berkeley, CA 94720, USA. Electronic address: fletch@berkeley.edu.
⁷ Department of Cellular and Molecular Pharmacology and Howard Hughes Medical Institute, University of California, San Francisco, Genentech Hall, 600 16(th) Street, San Francisco, CA 94158, USA. Electronic address: dyche.mullins@ucsf.edu.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Actin-Related Protein 2-3 Complex / metabolism*
Actins / chemistry*
Actins / metabolism*
Biomechanical Phenomena
Humans
Microscopy, Atomic Force
Microscopy, Fluorescence
Thermodynamics
Wiskott-Aldrich Syndrome Protein Family / chemistry
Wiskott-Aldrich Syndrome Protein Family / metabolism

Substances

Actin-Related Protein 2-3 Complex
Actins
WASF1 protein, human
Wiskott-Aldrich Syndrome Protein Family

Abstract

Publication types

MeSH terms

Substances

Grants and funding