Self-organized stress patterns drive state transitions in actin cortices

Tzer Han Tan, Maya Malik-Garbi, Enas Abu-Shah, Junang Li, Abhinav Sharma, Fred C. MacKintosh, Kinneret Keren*, Christoph F. Schmidt, Nikta Fakhri

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Biological functions rely on ordered structures and intricately controlled collective dynamics. This order in living systems is typically established and sustained by continuous dissipation of energy. The emergence of collective patterns of motion is unique to nonequilibrium systems and is a manifestation of dynamic steady states. Mechanical resilience of animal cells is largely controlled by the actomyosin cortex. The cortex provides stability but is, at the same time, highly adaptable due to rapid turnover of its components. Dynamic functions involve regulated transitions between different steady states of the cortex. We find that model actomyosin cortices, constructed to maintain turnover, self-organize into distinct nonequilibrium steady states when we vary cross-link density. The feedback between actin network structure and organization of stress-generating myosin motors defines the symmetries of the dynamic steady states. A marginally cross-linked state displays divergence-free long-range flow patterns. Higher cross-link density causes structural symmetry breaking, resulting in a stationary converging flow pattern. We track the flow patterns in the model actomyosin cortices using fluorescent single-walled carbon nanotubes as novel probes. The self-organization of stress patterns we have observed in a model system can have direct implications for biological functions.

Original languageEnglish
Article numbereaar2847
Pages (from-to)1-9
Number of pages9
JournalScience advances
Volume4
Issue number6
DOIs
Publication statusPublished - 6 Jun 2018

Funding

We thank A. Solon, J. Prost, S. Ramaswamy, M. Kardar, J. Gore, and A. Mogilner for discussion. This research was supported by a Sloan Research Fellowship (to N.F.), J.H. and E.V. Wade Fund Award (to N.F.), Human Frontier Science Program Career Development Award (to N.F.), the Cluster of Excellence and Deutsche Forschungsgemeinschaft (DFG) Research Center Nanoscale Microscopy and Molecular Physiology of the Brain (to C.F.S.), European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement n°340528 (to C.F.S.), the DFG Collaborative Research Center SFB 937 (Project A2; to C.F.S.), a grant from the Israel Science Foundation (grant no. 957/15; to K.K.), and the NSF (grant PHY-1427654; to F.C.M.). This work was also supported by funds from the Massachusetts Institute of Technology Department of Physics (to N.F.).

FundersFunder number
Human Frontier Science Program
Massachusetts Institute of Technology
Center for Nanoscale Science and TechnologyFP7/2007-2013
Seventh Framework Programme340528
Israel Science Foundation957/15, PHY-1427654

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